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Edited by Mark Estelle, University of California San Diego, La Jolla, CA, and approved July 16, 2020 (received for review April 1, 2020)
Significance
Plant seedlings depend on efficient development of roots and root hairs for anchorage to the ground and for rapidly reaching nutrients and water for survival and growth. We found that a negative regulator of a small-molecule signaling pathway called “karrikin signaling” plays an important role in regulating root growth of the legume Lotus japonicus. Mutants of this regulator called “SMAX1” have short primary roots and strongly elongated root hairs. This phenotype is caused by enhanced ethylene biosynthesis, which in the wild type is suppressed by SMAX1. Thus, karrikin signaling regulates ethylene biosynthesis to fine-tune root development.
Abstract
An evolutionarily ancient plant hormone receptor complex comprising the α/β-fold hydrolase receptor KARRIKIN INSENSITIVE 2 (KAI2) and the F-box protein MORE AXILLARY GROWTH 2 (MAX2) mediates a range of developmental responses to smoke-derived butenolides called karrikins (KARs) and to yet elusive endogenous KAI2 ligands (KLs). Degradation of SUPPRESSOR OF MAX2 1 (SMAX1) after ligand perception is considered to be a key step in KAR/KL signaling. However, molecular events which regulate plant development downstream of SMAX1 removal have not been identified. Here we show that Lotus japonicus SMAX1 is specifically degraded in the presence of KAI2 and MAX2 and plays an important role in regulating root and root hair development. smax1 mutants display very short primary roots and elongated root hairs. Their root transcriptome reveals elevated ethylene responses and expression of ACC Synthase 7 (ACS7), which encodes a rate-limiting enzyme in ethylene biosynthesis. smax1 mutants release increased amounts of ethylene and their root phenotype is rescued by treatment with ethylene biosynthesis and signaling inhibitors. KAR treatment induces ACS7 expression in a KAI2-dependent manner and root developmental responses to KAR treatment depend on ethylene signaling. Furthermore, in Arabidopsis, KAR-induced root hair elongation depends on ACS7. Thus, we reveal a connection between KAR/KL and ethylene signaling in which the KAR/KL signaling module (KAI2–MAX2–SMAX1) regulates the biosynthesis of ethylene to fine-tune root and root hair development, which are important for seedling establishment at the beginning of the plant life cycle.
Footnotes
↵1Present address: Department of Biology, University of Fribourg, 1700 Fribourg, Switzerland.
↵2Present address: State Key Laboratory of Agrobiotechnology (Shenzhen Base), Shenzhen Research Institute, The Chinese University of Hong Kong, Nanshan District, 518000 Shenzhen, China.
↵3Present address: Department of Plant and Microbial Biology, University of Zurich, 8008 Zurich, Switzerland.
- ↵4To whom correspondence may be addressed. Email: caroline.gutjahr{at}tum.de.
Author contributions: S.C. and C.G. designed research; S.C., K.V., M.C.K., and J.A.V.-A. performed research; S.C., K.V., J.A.V.-A., and C.G. analyzed data; D.D. analyzed RNA-sequencing data; and S.C. and C.G. wrote the paper.
The authors declare no competing interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2006111117/-/DCSupplemental.
Data Availability.
The RNA-seq data reported in this manuscript have been deposited in the National Center for Biotechnology Information database, https://dataview.ncbi.nlm.nih.gov/object/PRJNA591291?reviewer=vhn4av2bafiiutcnb53pd72ego (BioProject no. PRJNA591291). All study data are included in the article and SI Appendix.
Published under the PNAS license.
References
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The karrikin signaling regulator SMAX1 controls Lotus japonicus root and root hair development by suppressing ethylene biosynthesis
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