Structure-basis of signal ignition in spatial regulation of cell wall modification

Molecular mechanism for the recognition of sequence-divergent CIF peptides by the plant receptor kinases GSO1/SGN3 and GSO2

Satohiro Okuda*, Satoshi Fujita*, Andrea Moretti, Ulrich Hohmann, Verónica G. Doblas, Yan Ma, Alexandre Pfister, Benjamin Brandt, Niko Geldner, Michael Hothorn
*These authors are equally contributed to this work

Proceedings of the National Academy of Sciences PNAS first published January 21, 2020 DOI:10.1073/pnas.1911553117

Also available at BioRxiv doi

Higher plants develop Casparian strips in their roots to restrict simple diffusion of small molecules in their extracellular spaces to maintain homeostasis of whole plant bodies. Previous studies showed that a pair of receptor-kinase, GSO1(SGN3), and 21a.a.-sulfated peptides, CIF1/2, were required for Casparian strip maturation, but detail molecular mechanisms remained unclear.

Okuda and Fujita et al. presented a crystal structure of CIF2- GSO1(SGN3) peptide-receptor complex at 3 Å resolution. Quantitative analysis revealed that the GSO1(SGN3) and CIF2 pair had one of the highest affinities among known peptide-receptor pairs. Structure-based prediction uncovered Ile81 of CIF2 as a critical residue to form a tri-complex with newly identified co-receptors, SERK family proteins, to activate the downstream of the signaling pathway. Moreover, the structure-guided analysis identified homologs of CIF1/2, namely CIF3/4. CIF3/4 directly binds to GSO1(SGN3) and its homolog GSO2, but their binding properties are different from CIF1/2. Additionally, neither CIF3 nor 4 are expressing in root endodermal cells, where Casparian strips are made, implying these newly identified peptides play roles in different contexts. Our biochemical and developmental approaches provide a molecular framework to understand the recognition of diverse peptide hormones in plants.

This work was aided by grants no. 31003A_156261 and 310030E_176090 (N.G.), 31003A_176237 and 31CP30_180213 (M.H.) from the Swiss National Science Foundation, an ERC Consolidator Grant (616228-ENDOFUN) (N.G.), and an International Research Scholar Award from the Howard Hughes Medical Institute (M.H.), a Human Frontier Science Program Organization (HFSPO) postdoctoral fellowship no. LT000567/2016-L (S.O.) and a Japan Society for the Promotion of Science (JSPS) fellowship (S.F.).

Figure1

Figure: (A) Schematic model of Casparian strips (magenta). After establishing the connectivity (third row), this ring-like structure functions as an extracellular barrier. (Illustrated by Hiroko Uchida http://uchidahiroko.com/)
(B) Crystal structure of the GSO1(SGN3)/CIF2 receptor-peptide complex.


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