Developmental Functions of miR156-Regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) Genes in Arabidopsis thaliana

Abstract

Correct developmental timing is essential for plant fitness and reproductive success. Two important transitions in shoot development—the juvenile-to-adult vegetative transition and the vegetative-to-reproductive transition—are mediated by a group of genes targeted by miR156, SQUAMOSA PROMOTER BINDING PROTEIN (SBP) genes. To determine the developmental functions of these genes in Arabidopsis thaliana, we characterized their expression patterns, and their gain-of-function and loss-of-function phenotypes. Our results reveal that SBP-LIKE (SPL) genes in Arabidopsis can be divided into three functionally distinct groups: 1) SPL2, SPL9, SPL10, SPL11, SPL13 and SPL15 contribute to both the juvenile-to-adult vegetative transition and the vegetative-to-reproductive transition, with SPL9, SP13 and SPL15 being more important for these processes than SPL2, SPL10 and SPL11; 2) SPL3, SPL4 and SPL5 do not play a major role in vegetative phase change or floral induction, but promote the floral meristem identity transition; 3) SPL6 does not have a major function in shoot morphogenesis, but may be important for certain physiological processes. We also found that miR156-regulated SPL genes repress adventitious root development, providing an explanation for the observation that the capacity for adventitious root production declines as the shoot ages. miR156 is expressed at very high levels in young seedlings, and declines in abundance as the shoot develops. It completely blocks the expression of its SPL targets in the first two leaves of the rosette, and represses these genes to different degrees at later stages of development, primarily by promoting their translational repression. These results provide a framework for future studies of this multifunctional family of transcription factors, and offer new insights into the role of miR156 in Arabidopsis development.

Heteroblastic Development of Transfer Cells Is Controlled by the microRNA miR156/SPL Module

“…In agreement with levels of miR156 being high in young seedlings and gradually decreasing with plant age Xu et al, 2016aXu et al, , 2016b, we found that in mature shoots, juvenile leaves had significantly higher levels of miR156 compared to miR156 levels in transition and adult leaves (Fig. 5B).…”

“…SPL9-group genes have also been shown to function in flowering time Wu et al, 2009), with SPL15 playing a more important role than other SPL genes under long-d conditions (Xu et al, 2016a(Xu et al, , 2016b. In addition, other components of the flowering pathways including FLOWERING LOCUS C (FLC) and FLOWERING LOCUS T, also have effects on VPC and leaf morphology, and these effects can be either flowering-dependent or -independent (Willman and Poethig, 2011).…”

Transitioning to the Next Phase: The Role of Sugar Signaling throughout the Plant Life Cycle

“…Different signaling pathways may therefore exist (Matsoukas, 2014b;Hyun et al, 2017). Nevertheless, the juvenile-toadult phase transition and attainment of floral competence are both controlled by decreased expression of miR156 and increased expression of its targets, the group of SBP/SPL transcription factor genes (Wu and Poethig, 2006;Wu et al, 2009;Xu et al, 2016; Fig. 1).…”

“…While there is overlap in SPL function, different members of the SPL transcription factor family also have specific developmental functions in vegetative phase change and the floral transition (Xu et al, 2016).…”

The hot, the cold and the tulip : the regulation of flowering time and dormancy release

“…An important regulator of maintaining the juvenile vegetative phase, by repression of SQUAMOSA PROMOTOR BINDING PROTEIN LIKE (SPL) genes, is micro RNA 156 (miR156). Only repression of this miRNA in the shoot, initiated by a leaf derived signal, will result in the vegetative phase change by activation of its targets SPL9, SPL13 and SPL15 Yang et al, 2010;Xu et al, 2016). The miR156/ SPL module is conserved and this has been functionally confirmed in e.g.…”