Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission.

Julia Santiago,Ludwig A Hothorn,Benjamin Brandt,Ulrich Hohmann,Michael Hothorn,Mari Wildhagen,Melinka A Butenko

doi:10.7554/elife.15075

Julia Santiago, Ludwig A Hothorn + Show 5 more

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https://doi.org/10.7554/elife.15075

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Abstract

Plants constantly renew during their life cycle and thus require to shed senescent and damaged organs. Floral abscission is controlled by the leucine-rich repeat receptor kinase (LRR-RK) HAESA and the peptide hormone IDA. It is unknown how expression of IDA in the abscission zone leads to HAESA activation. Here we show that IDA is sensed directly by the HAESA ectodomain. Crystal structures of HAESA in complex with IDA reveal a hormone binding pocket that accommodates an active dodecamer peptide. A central hydroxyproline residue anchors IDA to the receptor. The HAESA co-receptor SERK1, a positive regulator of the floral abscission pathway, allows for high-affinity sensing of the peptide hormone by binding to an Arg-His-Asn motif in IDA. This sequence pattern is conserved among diverse plant peptides, suggesting that plant peptide hormone receptors may share a common ligand binding mode and activation mechanism.

Highlights

During their growth, development and reproduction plants use cell separation processes to detach no-longer required, damaged or senescent organs
We find many of the residues contributing to the formation of the IDA binding surface in HAESA to be conserved in HAESA-LIKE 2 (HSL2) and in other HAESAtype receptors in different plant species (Figure 1—figure supplement 3)
We found that the force required to remove the petals of serk1-1 mutants is significantly higher than that needed for wildtype plants, as previously observed for haesa/hsl2 mutants (Stenvik et al, 2008), and that floral abscission is delayed in serk1-1 (Figure 3A)

Summary

Introduction

Development and reproduction plants use cell separation processes to detach no-longer required, damaged or senescent organs. Full-length IDA is proteolytically processed and a conserved stretch of 20 amino-acids (termed EPIP) can rescue the IDA loss-of-function phenotype (Figure 1A) (Stenvik et al, 2008). It has been demonstrated that a dodecamer peptide within EPIP is able to activate HAESA and HSL2 in transient assays in tobacco cells (Butenko et al, 2014). This sequence motif is highly conserved among IDA family members (IDA-LIKE PROTEINS, IDLs) and contains a central Pro residue, presumed to be post-translationally modified to hydroxyproline (Hyp; Figure 1A) (Butenko et al, 2003; 2014). The available genetic and biochemical evidence suggests that IDA and HAESA together control floral abscission, but it is poorly understood if IDA is directly sensed by the receptor kinase HAESA and how IDA binding at the cell surface would activate the receptor

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