An Intrinsic MicroRNA Timer Regulates Progressive Decline in Shoot Regenerative Capacity in Plants

Abstract

Plant cells are totipotent and competent to regenerate from differentiated organs. It has been shown that two phytohormones, auxin and cytokinin, play critical roles within this process. As in animals, the regenerative capacity declines with age in plants, but the molecular basis for this phenomenon remains elusive. Here, we demonstrate that an age-regulated microRNA, miR156, regulates shoot regenerative capacity. As a plant ages, the gradual increase in miR156-targeted SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) transcription factors leads to the progressive decline in shoot regenerative capacity. In old plants, SPL reduces shoot regenerative capacity by attenuating the cytokinin response through binding with the B-type ARABIDOPSIS RESPONSE REGULATORs, which encode the transcriptional activators in the cytokinin signaling pathway. Consistently, the increased amount of exogenous cytokinin complements the reduced shoot regenerative capacity in old plants. Therefore, the recruitment of age cues in response to cytokinin contributes to shoot regenerative competence.

Transcriptomic Signature of the SHATTERPROOF2 Expression Domain Reveals the Meristematic Nature of Arabidopsis Gynoecial Medial Domain

“…The SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE (SPL) genes function in the regulation of the transition from juvenile to adult growth phases and the regulation of shoot regenerative capacity (Wu and Poethig, 2006;Wang et al, 2008Wang et al, , 2009Zhang et al, 2015). In our study, the expression of SPL3 (AT2G33810) was more than 4-fold lower in the YFP-positive sample relative to the YFP-negative sample.…”

Plant regeneration: cellular origins and molecular mechanisms

“…Explants from juvenile plants regenerate shoots more effectively than those from mature plants (Dong and Jia, 1991;Baker and Bhatia, 1993;Becerra et al, 2004;Zhang et al, 2015). The decline in shoot regeneration capacity with aging is at least partly due to a reduced responsiveness to plant hormones.…”

“…The decline in shoot regeneration capacity with aging is at least partly due to a reduced responsiveness to plant hormones. The microRNA miR156 has been shown to regulate the juvenile-to-adult phase transition in plants (Wu et al, 2009), and a recent study suggests that a decline of miR156 expression in old plants is responsible for reduced shoot regeneration (Zhang et al, 2015). This reduction in miR156 increases the level of its target SQUAMOSA PROMOTER BINDING-LIKE9 (SPL9).…”

“…This reduction in miR156 increases the level of its target SQUAMOSA PROMOTER BINDING-LIKE9 (SPL9). SPL9, in turn, inhibits the transcriptional activity of B-type ARABIDOPSIS RESPONSE REGULATOR proteins (ARRs), leading to the reduced responsiveness to cytokinin and hence compromised shoot regeneration (Zhang et al, 2015).…”

Type-B ARABIDOPSIS RESPONSE REGULATORs Specify the Shoot Stem Cell Niche by Dual Regulation of WUSCHEL

“…The expression of Arabidopsis His kinases4, which encodes a cytokinin receptor, precedes and subsequently overlaps with that of WUS (Gordon et al, 2009). Mutations in type-B ARABIDOPSIS RESPONSE REGULATORs (ARRs), key regulators of primary cytokinin response genes, result in reduced shoot regeneration (Ishida et al, 2008;Hwang et al, 2012;Hill et al, 2013;Zhang et al, 2015). By contrast, overexpressing type-A ARRs encoding negative regulators of cytokinin signaling suppress shoot formation (Buechel et al, 2010).…”