The HB40-JUB1 transcriptional regulatory network controls gibberellin homeostasis in Arabidopsis

Shuchao Dong,Danuse Tarkowska,Mastoureh Sedaghatmehr,Maryna Welsch,Saurabh Gupta,Bernd Mueller-Roeber,Salma Balazadeh

doi:10.1016/j.molp.2021.10.007

Shuchao Dong, Danuse Tarkowska + Show 5 more

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The gibberellins (GAs) are phytohormones that play fundamental roles in almost every aspect of plant growth and development. Although GA biosynthetic and signaling pathways are well understood, the mechanisms that control GA homeostasis remain largely unclear in plants. Here, we demonstrate that the homeobox transcription factor (TF) HB40 of the HD-Zip family regulates GA content at two additive control levels in Arabidopsis thaliana. We show that HB40 expression is induced by GA and in turn reduces the levels of endogenous bioactive GAs by simultaneously reducing GA biosynthesis and increasing GA deactivation. Consistently, HB40 overexpression leads to typical GA-deficiency traits, such as small rosettes, reduced plant height, delayed flowering, and male sterility. By contrast, a loss-of-function hb40 mutation enhances GA-controlled growth. Genome-wide RNA sequencing combined with molecular-genetic analyses revealed that HB40 directly activates the transcription of JUNGBRUNNEN1 (JUB1), a key TF that represses growth by suppressing GA biosynthesis and signaling. HB40 also activates genes encoding GA 2-oxidases (GA2oxs), which are major GA-catabolic enzymes. The effect of HB40 on plant growth is ultimately mediated through the induction of nuclear growth-repressing DELLA proteins. Collectively, our results reveal the important role of the HB40-JUB1 regulatory network in controlling GA homeostasis during plant growth.

Highlights

Gibberellins (GAs) are essential plant hormones regulating virtually all aspects of the plant’s life including, inter alia, seed germination, hypocotyl and stem elongation, leaf expansion and flower development (Achard and Genschik 2009; Hedden and Sponsel 2015; Binenbaum et al 2018)
We show that HOMEOBOX PROTEIN 40 (HB40) expression is induced by GA and in turn reduces the levels of endogenous bioactive GAs by a simultaneous reduction of GA biosynthesis and increased GA deactivation
The key roles of GA in the regulation of plant growth and development indicate that dynamic modulation of its homeostasis is crucial throughout the entire plants’ life cycles

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INTRODUCTION

Gibberellins (GAs) are essential plant hormones regulating virtually all aspects of the plant’s life including, inter alia, seed germination, hypocotyl and stem elongation, leaf expansion and flower development (Achard and Genschik 2009; Hedden and Sponsel 2015; Binenbaum et al 2018). HB40 Directly and Positively Regulates JUB1 To identify putative HB40 targets we first used RNA-seq and compared the transcriptomes of plants expressing HB40 protein (fused to hemagglutinin/HA tag) from an estradiol (Est)inducible promoter (hereafter, HB40-HA-IOE; 2 h Est treatment) (Gonzalez-Grandio et al. Journal Pre-proof 2017) with those of mock-treated controls. We found that the jub knockdown mutation largely rescues the phenotypes of HB40-overexpressing plants from their signature defects of shorter hypocotyls, smaller rosettes, dwarfism, and delayed flowering (Figure 2I-L and Supplemental Figure 5B-5F) without changing the low JUB1 expression of the mutant background This result clearly demonstrates that HB40 requires functional JUB1 for growth control. Treatment with BL had no significant effect in the light, and only a weak effect in Journal Pre-proof the dark (even at high concentration, 1 M) on hypocotyls of HB40OX

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