SMAX1/SMXL2 regulate root and root hair development downstream of KAI2-mediated signalling in Arabidopsis.

José Antonio Villaécija-Aguilar,Caroline Gutjahr,Samy Carbonnel,Tom Bennett,Christian Schmidt,Maxime Hamon-Josse,Corinna Dawid,Annika Kretschmar,Gloria K Muday

doi:10.1371/journal.pgen.1008327

Abstract

Karrikins are smoke-derived compounds presumed to mimic endogenous signalling molecules (KAI2-ligand, KL), whose signalling pathway is closely related to that of strigolactones (SLs), important regulators of plant development. Both karrikins/KLs and SLs are perceived by closely related α/β hydrolase receptors (KAI2 and D14 respectively), and signalling through both receptors requires the F-box protein MAX2. Furthermore, both pathways trigger proteasome-mediated degradation of related SMAX1-LIKE (SMXL) proteins, to influence development. It has previously been suggested in multiple studies that SLs are important regulators of root and root hair development in Arabidopsis, but these conclusions are based on phenotypes observed in the non-specific max2 mutants and by use of racemic-GR24, a mixture of stereoisomers that activates both D14 and KAI2 signalling pathways. Here, we demonstrate that the majority of the effects on Arabidopsis root development previously attributed to SL signalling are actually mediated by the KAI2 signalling pathway. Using mutants defective in SL or KL synthesis and/or perception, we show that KAI2-mediated signalling alone regulates root hair density and root hair length as well as root skewing, straightness and diameter, while both KAI2 and D14 pathways regulate lateral root density and epidermal cell length. We test the key hypothesis that KAI2 signals by a non-canonical receptor-target mechanism in the context of root development. Our results provide no evidence for this, and we instead show that all effects of KAI2 in the root can be explained by canonical SMAX1/SMXL2 activity. However, we do find evidence for non-canonical GR24 ligand-receptor interactions in D14/KAI2-mediated root hair development. Overall, our results demonstrate that the KAI2 signalling pathway is an important new regulator of root hair and root development in Arabidopsis and lay an important basis for research into a molecular understanding of how very similar and partially overlapping hormone signalling pathways regulate different phenotypic outputs.

Highlights

Plant roots continually integrate environmental information to make decisions about their development, and to optimize their growth for optimal nutrient uptake and anchorage
Perception of karrikins/KL is very similar to that of another plant hormone class, strigolactones (SLs). Both hormones bind to the related α/β-fold hydrolase receptors KAI2 and D14 respectively, which both interact with the F-box protein MORE AXILLIARY BRANCHES2 (MAX2), for ubiquitylation and subsequent degradation of KL- or SL-signalling specific proteins of the SMXL family
We genetically dissected the role of KL and SL signalling in root and root hair development in Arabidopsis seedlings and show that most root traits are regulated by KL and not by SL signaling: lateral root density is controlled by KL and SL signalling together, while root growth direction, root straightness and root hair development are determined by KL signalling alone

Summary

Introduction

Plant roots continually integrate environmental information to make decisions about their development, and to optimize their growth for optimal nutrient uptake and anchorage. Root development is regulated by a number of phytohormones, low-molecular-weight signalling molecules, which mediate localized developmental responses as well as transmission and integration of information across long distances. SLs have been suggested to act as important regulators of Arabidopsis seedling root architecture and root hair development [6,7,8,9]. The exact role of SLs in root development remains uncertain, due to interpretational difficulties inherent in the materials used by those studies, namely max mutants and the synthetic strigolactone racemic-GR24 (see below, [10]). D14 interacts with the SCFMAX2 E3 ubiquitin ligase complex to induce ubiquitylation and subsequent degradation of target proteins, essential to trigger SL signal transduction [15, 17]

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