Strigolactone and Karrikin Signaling Pathways Elicit Ubiquitination and Proteolysis of SMXL2 to Regulate Hypocotyl Elongation in Arabidopsis.

Haiyan Ma,Steven M. Smith,Yonghong Wang,Hong Yu,Qi Xie,Jiayang Li,Bing Wang,Guosheng Xiong,Jun Yang,Xiaoqiang Li,Lei Wang,Qian Xu,Jinfang Chu

doi:10.1105/tpc.20.00140

Abstract

Strigolactones (SLs) and karrikins (KARs) are related butenolide signaling molecules that control plant development. In Arabidopsis (Arabidopsis thaliana), they are recognized separately by two closely related receptors but use the same F-box protein MORE AXILLARY GROWTH2 (MAX2) for signal transduction, targeting different members of the SMAX1-LIKE (SMXL) family of transcriptional repressors for degradation. Both signals inhibit hypocotyl elongation in seedlings, raising the question of whether signaling is convergent or parallel. Here, we show that synthetic SL analog GR244DO enhanced the interaction between the SL receptor DWARF14 (D14) and SMXL2, while the KAR surrogate GR24 ent-5DS induced association of the KAR receptor KARRIKIN INSENSITIVE2 (KAI2) with SMAX1 and SMXL2. Both signals trigger polyubiquitination and degradation of SMXL2, with GR244DO dependent on D14 and GR24 ent-5DS dependent mainly on KAI2. SMXL2 is critical for hypocotyl responses to GR244DO and functions redundantly with SMAX1 in hypocotyl response to GR24 ent-5DS Furthermore, GR244DO induced response of D14-LIKE2 and KAR-UP F-BOX1 through SMXL2, whereas GR24 ent-5DS induced expression of these genes via both SMAX1 and SMXL2. These findings demonstrate that both SLs and KARs could trigger polyubiquitination and degradation of SMXL2, thus uncovering an unexpected but important convergent pathway in SL- and KAR-regulated gene expression and hypocotyl elongation.

Highlights

Strigolactones (SLs) are a large diverse group of signaling compounds derived from the carotenoid biosynthetic pathway and possess a characteristic butenolide ring that is essential for activity
To investigate the specific gene expression responding to SLs, we used GR244DO as an active SL analog because our preliminary studies showed it to be more active than GR245DS
SMXL2 Is Involved in Both SL and KAR Signaling Pathways Based on findings in this and earlier studies, we propose an overview model of SL and KAR signaling in Arabidopsis (Figure 9)

Summary

Introduction

Strigolactones (SLs) are a large diverse group of signaling compounds derived from the carotenoid biosynthetic pathway and possess a characteristic butenolide ring that is essential for activity They function in many aspects of plant development, such as shoot branching, internode elongation, leaf elongation and senescence, growth of primary and lateral roots, anthocyanin accumulation, shoot gravitropism, and stem secondary thickening (Foo et al, 2001; Stirnberg et al, 2002; Sorefan et al, 2003; Snowden et al., 2005; Arite et al, 2007; Simons et al, 2007; Gomez-Roldan et al, 2008; Umehara et al., 2008; Drummond et al, 2009; Lin et al, 2009; Agusti et al, 2011; Sang et al, 2014). Due to the important roles of SLs in key agronomic traits related to crop yield and mechanized farming, it is important to understand the molecular mechanism of SL action in plants

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