Threshold-dependent repression of SPL gene expression by miR156/miR157 controls vegetative phase change in Arabidopsis thaliana

Abstract

Vegetative phase change is regulated by a decrease in the abundance of the miRNAs, miR156 and miR157, and the resulting increase in the expression of their targets, SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) transcription factors. To determine how miR156/miR157 specify the quantitative and qualitative changes in leaf morphology that occur during vegetative phase change, we measured their abundance in successive leaves and characterized the phenotype of mutations in different MIR156 and MIR157 genes. miR156/miR157 decline rapidly between leaf 1&2 and leaf 3 and decrease more slowly after this point. The amount of miR156/miR157 in leaves 1&2 greatly exceeds the threshold required to specify their identity. Subsequent leaves have relatively low levels of miR156/miR157 and are sensitive to small changes in their abundance. In these later-formed leaves, the amount of miR156/miR157 is close to the threshold required to specify juvenile vs. adult identity; a relatively small decrease in the abundance of miR156/157 in these leaves produces a disproportionately large increase in SPL proteins and a significant change in leaf morphology. miR157 is more abundant than miR156 but has a smaller effect on shoot morphology and SPL gene expression than miR156. This may be attributable to the inefficiency with which miR157 is loaded onto AGO1, as well as to the presence of an extra nucleotide at the 5' end of miR157 that is mis-paired in the miR157:SPL13 duplex. miR156 represses different targets by different mechanisms: it regulates SPL9 by a combination of transcript cleavage and translational repression and regulates SPL13 primarily by translational repression. Our results offer a molecular explanation for the changes in leaf morphology that occur during shoot development in Arabidopsis and provide new insights into the mechanism by which miR156 and miR157 regulate gene expression.

TEMPRANILLO is a direct repressor of the microRNA miR172

“…There is feedback regulation of SPL genes by miR172 target genes, such that miR172 target genes negatively regulate several SPLs or positively regulate miR156 (Yant et al, 2010;Jung et al, 2011). This indirect feedback on miR156 might result in the observed differential effect on SPL expression, as the SPL3 transcript has recently been shown to be more sensitive to miR156 cleavage than SPL9 or SPL15 (He et al, 2018). It is possible, therefore, that the downregulation of SPL3 and SPL9 observed in 35S::TEM1 plants (Figure 5a-i) is an indirect consequence of the downregulation of miR172 (Figure 6b)and the expected upregulation of miR172 targetsin these plants.…”

Do ArabidopsisSquamosa promoter binding Protein‐Likegenes act together in plant acclimation to copper or zinc deficiency?

“…The levels of miR156 decline with progressive plant development (Wang, Czech, & Weigel, ; Wu et al., ; Wu & Poethig, ), which leads to a gradual increase in the expression of miR156‐targeted SPLs. This constitutes a regulatory module in diverse developmental processes such as developmental phase transition, the specification of floral meristem identity, shoot branching, and lateral root development (Wu & Poethig, ; Schwarz, Grande, Bujdoso, Saedler, & Huijser, ; Wu et al., ; Yamaguchi et al., ; Yu, Niu, Ng, & Chua, ; Xu et al., ; He et al., ).…”

“…This constitutes a regulatory module in diverse developmental processes such as developmental phase transition, the specification of floral meristem identity, shoot branching, and lateral root development (Wu & Poethig, 2006;Schwarz, Grande, Bujdoso, Saedler, & Huijser, 2008;Wu et al, 2009;Yamaguchi et al, 2009;Yu, Niu, Ng, & Chua, 2015;Xu et al, 2016;He et al, 2018).…”

Do Arabidopsis Squamosa promoter binding Protein-Like genes act together in plant acclimation to copper or zinc deficiency?

“…The levels of miR156 decline with progressive plant development Wu et al 2009;Wu and Poethig 2006), which leads to a gradual increase in the expression of miR156-targeted SPLs. This constitutes a regulatory module in diverse developmental processes such as developmental phase transition, the specification of floral meristem identity, shoot branching and lateral root development (Wu and Poethig 2006;Schwarz et al 2008;Wu et al 2009;Yamaguchi et al 2009;Yu et al 2015;Xu et al 2016;He et al 2018).…”