Research Article: Crystal structures of two tandem malectin-like receptor kinases involved in plant reproduction

Date Published: July 01, 2018

Publisher: International Union of Crystallography

Author(s): Steven Moussu, Sebastian Augustin, Andra-Octavia Roman, Caroline Broyart, Julia Santiago.


The biochemical and crystallographic characterization of different Catharanthus roseus receptor kinase 1-like membrane receptors is reported as a first step to understand cell-wall sensing and signalling mechanisms in plants.

Partial Text

Plant cells are surrounded by a dynamic, carbohydrate-rich cell wall which is constantly remodelled to enable coordinated growth and development, and serves as a link to the outside world (Ringli, 2010 ▸). To sense and integrate environmental and internal signals, plants have evolved a set of membrane receptor kinases (RKs), the extracellular domains of which face the cell-wall compartment (Shiu & Bleecker, 2001 ▸, 2003 ▸). Members of the plant-specific Catharanthus roseus receptor kinase 1-like (CrRLK1L) family are key players in monitoring the cell-wall status and regulating cell expansion (Voxeur & Höfte, 2016 ▸; Wolf et al., 2012 ▸; Boisson-Dernier et al., 2011 ▸). Of the 17 members in Arabidopsis, ten have been functionally characterized: FERONIA (FER), ANXUR1 (ANX1), ANXUR2 (ANX2), BUDDHA PAPER SEAL 1/2 (BUPS1/2), HERCULES1 (HERK1), HERCULES2 (HERK2), [Ca2+]cyt-associated protein kinase 1 (CAP1/ERULUS), THESEUS1 (THE1) and CURVY1 (CVY1) (Nissen et al., 2016 ▸). FER, ANX1/2 and BUPS1/2 are involved in cell-communication events regulating plant fertilization, with FER acting in the female gametophyte and ANX1/2 and BUPS1/2 in the male gametophyte, the pollen. Loss of FER function impairs pollen-tube reception (Escobar-Restrepo et al., 2007 ▸), whereas ANX1/2, together with BUPS1/2, helps to maintain pollen-tube integrity during polarized tip growth, assuring fertilization (Boisson-Dernier et al., 2009 ▸; Ge et al., 2017 ▸; Miyazaki et al., 2009 ▸). FER, THE1, HERK1 and HERK2 have been implicated in regulating cell expansion during vegetative growth (Guo, Ye et al., 2009 ▸; Guo, Li et al., 2009 ▸), with FER having additional roles in plant immunity (Keinath et al., 2010 ▸; Kessler et al., 2010 ▸; Stegmann et al., 2017 ▸). THE1 has been described to be able to sense structural changes in the cell wall and to regulate lignin accumulation in cellulose-deficient mutants (Hématy et al., 2007 ▸). Recent studies have also linked a member of this receptor family to the control of cell morphogenesis and cytoskeleton assembly (Gachomo et al., 2014 ▸).

Genetic studies have revealed important functions for the plant-unique CrRLK1L membrane receptor kinases in very different physiological processes ranging from plant reproduction, cell elongation and growth to immunity (Li et al., 2016 ▸; Nissen et al., 2016 ▸). CrRLK1Ls may regulate all of these different processes by controlling specific signalling events that lead to remodelling of the cell wall. Based on their distant sequence homology to animal carbohydrate-binding modules, the ectodomains of CrRLK1Ls were originally proposed to bind carbohydrate ligands (Li et al., 2016 ▸; Voxeur & Höfte, 2016 ▸). The structures of ANX1 and ANX2 reveal an un­expected novel fold with the two malectin-like domains packed against each other and connected by a short β-hairpin linker, forming a potential ligand-binding cleft. Similar results have recently been reported by Du et al. (2018 ▸) in an independent study. In the case of ANX1 the crystals from both studies were isomorphous (r.m.s.d. of 0.6 Å over 382 corresponding Cα atoms) and grew in similar conditions, with our crystals diffracting to higher resolution (1.48 Å). In our hands, the ANX2 receptor crystallized in a different crystal form and diffracted to 1.1 Å resolution. Comparison of the ANX2 structures resulted in an r.m.s.d. value of 0.5 Å over 377 corresponding Cα atoms.




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