Cytokinin regulates vegetative phase change in Arabidopsis thaliana through the miR172/TOE1-TOE2 module

Sören Werner,Isabel Bartrina,Thomas Schmülling

doi:10.1038/s41467-021-26088-z

Sören Werner, Isabel Bartrina + Show 1 more

Open Access

https://doi.org/10.1038/s41467-021-26088-z

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Abstract

During vegetative growth plants pass from a juvenile to an adult phase causing changes in shoot morphology. This vegetative phase change is primarily regulated by the opposite actions of two microRNAs, the inhibitory miR156 and the promoting miR172 as well as their respective target genes, constituting the age pathway. Here we show that the phytohormone cytokinin promotes the juvenile-to-adult phase transition through regulating components of the age pathway. Reduction of cytokinin signalling substantially delayed the transition to the adult stage. tZ-type cytokinin was particularly important as compared to iP- and the inactive cZ-type cytokinin, and root-derived tZ influenced the phase transition significantly. Genetic and transcriptional analyses indicated the requirement of SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) transcription factors and miR172 for cytokinin activity. Two miR172 targets, TARGET OF EAT1 (TOE1) and TOE2 encoding transcriptional repressors were necessary and sufficient to mediate the influence of cytokinin on vegetative phase change. This cytokinin pathway regulating plant aging adds to the complexity of the regulatory network controlling the juvenile-to-adult phase transition and links cytokinin to miRNA action.

Highlights

During vegetative growth plants pass from a juvenile to an adult phase causing changes in shoot morphology
Comparing the leaf morphology of mutants with a lower CK status like the CK receptor mutant ahk[2] ahk[3] and plants overexpressing the CKdegrading enzyme CKX1 (CKX1ox) with wild type, we observed a larger number of leaves with juvenile features (Fig. 1)
In order to investigate the possible influence of CK on vegetative phase change, we examined the appearance of abaxial trichomes in CKX1ox and ahk[2] ahk[3], as well as in ckx[3,4,5,6] and the ARABIDOPSIS HISTIDINE KINASE2 (AHK2) gain-of-function mutant rock[248] as plants with an increased CK content or signaling, respectively

Summary

Introduction

During vegetative growth plants pass from a juvenile to an adult phase causing changes in shoot morphology. Two miR172 targets, TARGET OF EAT1 (TOE1) and TOE2 encoding transcriptional repressors were necessary and sufficient to mediate the influence of cytokinin on vegetative phase change. This cytokinin pathway regulating plant aging adds to the complexity of the regulatory network controlling the juvenile-to-adult phase transition and links cytokinin to miRNA action. MOTER BINDING PROTEIN-LIKE (SPL) genes, a group of transcription factor genes controlling several aspects of Arabidopsis shoot development, such as the timing of juvenile-to-adult and vegetative-to-reproductive phase transitions, leaf initiation rate, and floral organ development[14,15,16].

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