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

First author: José Antonio Villaécija-Aguilar; Affiliations: Technical University of Munich (慕尼黑理工大学): Freising, Germany

Corresponding author: Caroline Gutjahr

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 lays an important basis for research into a molecular understanding of how very similar and partially overlapping hormone signalling pathways regulate different phenotypic outputs.

Karrikins是源自于烟的一种化合物，其能够模仿植物内源的信号分子KAI2配基KL，其信号通路与独角金内酯SL十分近似，对于植物的发育起到重要的调控作用。karrikins/KLs和SLs分别由植物的α/β水解酶受体KAI2和D14所感知，并且通过这两个受体的信号通路均需要一个F-box蛋白MAX2的参与。此外，这两个通路均能够诱导蛋白酶体介导的相关类SMAX1蛋白SMXL的降解，从而影响植物发育。有很多研究都显示独角金内酯SL对于拟南芥的根和根毛的发育起到关键的调控作用，但这些研究均是基于非特异性max2突变体的表型数据以及利用一个能够同时影响D14和KAI2信号通路的立体异构体混合物外消旋GR24所得结果推测而来的。本文中，作者的研究显示之前的研究中所认为的SL信号通路介导的拟南芥根发育调控大多是由KAI2信号通路所介导的。利用SL或KL合成或感知突变体，作者发现单独KAI2介导的信号通路就能够调控根毛密度和根毛长度，同时还能够影响根的弯曲、直度以及直径，而KAI2和D14通路均能够调控侧根密度和表皮细胞长度。作者在根发育的背景下测试了KAI2信号是否由非典型受体靶向机制所介导，结果显示没有相关的证据能够说明这一点，相反，作者的试验显示所有KAI2对于根的影响均能够用经典的SMAX1/SMXL2活动来解释。然而，作者确实在D14/KAI2介导的根毛发育过程中发现了非典型的GR24配基-受体互作。综上，本文的研究结果揭示了KAI2信号通路是一个新的调控拟南芥根和根毛发育的因子，并且提供了一个如何区分相似或部分重叠的激素信号通路调控不同表型的研究思路。

通讯：Caroline Gutjahr（https://www.professoren.tum.de/en/gutjahr-caroline/)

个人简介：1997-2003年，德国弗赖堡大学和苏格兰阿伯丁大学，学士；2005-2010年，瑞士日内瓦大学和洛桑大学，博士；2010-2011年，瑞士洛桑大学，博士后。

研究方向：植物-真菌共生系统中的植物激素与转录调控网络。

doi: https://doi.org/10.1371/journal.pgen.1008327

Journal: PLOS Genetics

Published online: August 29, 2019