MiR824/AGAMOUS-LIKE16 Module Integrates Recurring Environmental Heat Stress Changes to Fine-Tune Poststress Development.

Henrik Mihály Szaker,Éva Darkó,Yee-Yung Charng,Tibor Janda,Hsiang-Chin Liu,Tibor Csorba,Anna Medzihradszky

doi:10.3389/fpls.2019.01454

Abstract

Plant development is continually fine-tuned based on environmental factors. How environmental perturbations are integrated into the developmental programs and how poststress adaptation is regulated remains an important topic to dissect. Vegetative to reproductive phase change is a very important developmental transition that is complexly regulated based on endogenous and exogenous cues. Proper timing of flowering is vital for reproductive success. It has been shown previously that AGAMOUS LIKE 16 (AGL16), a MADS-box transcription factor negatively regulates flowering time transition through FLOWERING LOCUS T (FT), a central downstream floral integrator. AGL16 itself is negatively regulated by the microRNA miR824. Here we present a comprehensive molecular analysis of miR824/AGL16 module changes in response to mild and recurring heat stress. We show that miR824 accumulates gradually in response to heat due to the combination of transient transcriptional induction and posttranscriptional stability. miR824 induction requires heat shock cis-elements and activity of the HSFA1 family and HSFA2 transcription factors. Parallel to miR824 induction, its target AGL16 is decreased, implying direct causality. AGL16 posttranscriptional repression during heat stress, however, is more complex, comprising of a miRNA-independent, and a miR824-dependent pathway. We also show that AGL16 expression is leaf vein-specific and overlaps with miR824 (and FT) expression. AGL16 downregulation in response to heat leads to a mild derepression of FT. Finally, we present evidence showing that heat stress regulation of miR824/AGL16 is conserved within Brassicaceae. In conclusion, due to the enhanced post-transcriptional stability of miR824, stable repression of AGL16 is achieved following heat stress. This may serve to fine-tune FT levels and alter flowering time transition. Stress-induced miR824, therefore, can act as a “posttranscriptional memory factor” to extend the acute impact of environmental fluctuations in the poststress period.

Highlights

In nature, plants adapt to the diurnally and seasonally fluctuating environment for successful growth and reproduction
ACC: Gradient acclimation was done in the presence of light in a water bath in the course of 4 h: the temperature was rose starting at Zeitgeber Time ZT4 and reached 37°C at ZT7; plants were kept on 37°C for 1 h from ZT7 to Zeitgeber Time 8 (ZT8)
We hypothesized that due to their high stability, the stress-responsive miRNAs might gradually accumulate in response to recurring stress cues and act as lasting memory factors to fine-tune their targets on longer terms after stress

Summary

Introduction

Plants adapt to the diurnally and seasonally fluctuating environment for successful growth and reproduction. One important task of the HSR signal transduction pathways is the activation of HS transcription factors (HSFs) (Mittler et al, 2012; Scharf et al, 2012; Yeh et al, 2012). Acclimation occurs gradually during the day and repeatedly at the beginning of the hot season. This so-called acquired thermotolerance allows plants to survive upcoming stronger, even lethal stresses (Mittler et al, 2012; Lamke and Baurle, 2017; Liu et al, 2018). While the different forms of HSR have been intensively studied, how plants integrate sporadic or repeated stress signals and alter their development following stress is much less known

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