TY - JOUR

T1 - HSL1 and BAM1/2 impact epidermal cell development by sensing distinct signaling peptides

AU - Roman, Andra-Octavia

AU - Jimenez-Sandoval, Pedro

AU - Augustin, Sebastian

AU - Broyart, Caroline

AU - Hothorn, Ludwig A.

AU - Santiago, Julia

N1 - Funding Information: The authors thank V. Olieric for providing beam-time and the staff at beam-line PXIII of the Swiss Light Source (SLS), Villigen, for technical assistance during data collection. Special thanks to Zachary Nimchuck (University of North Carolina) for providing us with bam1-4 bam2-4 mutant and Christian Hardtke (University of Lausanne) for the pBAM1::3xNLS::YFP reporter line. We would also like to thank Anaxi Houbaert for his input and help to set up the epidermal cell quantification, and to Yan Ma for helping us with R functions. Supported by the University of Lausanne, Swiss National Science Foundation grants no. 31003A_173101, the European Research Council (ERC) grant agreement no. 716358 and the Fondation Philanthropique Famille Sandoz.

PY - 2022/12

Y1 - 2022/12

N2 - The membrane receptor kinases HAESA and HSL2 recognize a family of IDA/IDL signaling peptides to control cell separation processes in different plant organs. The homologous HSL1 has been reported to regulate epidermal cell patterning by interacting with a different class of signaling peptides from the CLE family. Here we demonstrate that HSL1 binds IDA/IDL peptides with high, and CLE peptides with lower affinity, respectively. Ligand sensing capability and receptor activation of HSL1 require a SERK co-receptor kinase. Crystal structures with IDA/IDLs or with CLE9 reveal that HSL1-SERK1 complex recognizes the entire IDA/IDL signaling peptide, while only parts of CLE9 are bound to the receptor. In contrast, the receptor kinase BAM1 interacts with the entire CLE9 peptide with high affinity and specificity. Furthermore, the receptor tandem BAM1/BAM2 regulates epidermal cell division homeostasis. Consequently, HSL1-IDLs and BAM1/BAM2-CLEs independently regulate cell patterning in the leaf epidermal tissue.

AB - The membrane receptor kinases HAESA and HSL2 recognize a family of IDA/IDL signaling peptides to control cell separation processes in different plant organs. The homologous HSL1 has been reported to regulate epidermal cell patterning by interacting with a different class of signaling peptides from the CLE family. Here we demonstrate that HSL1 binds IDA/IDL peptides with high, and CLE peptides with lower affinity, respectively. Ligand sensing capability and receptor activation of HSL1 require a SERK co-receptor kinase. Crystal structures with IDA/IDLs or with CLE9 reveal that HSL1-SERK1 complex recognizes the entire IDA/IDL signaling peptide, while only parts of CLE9 are bound to the receptor. In contrast, the receptor kinase BAM1 interacts with the entire CLE9 peptide with high affinity and specificity. Furthermore, the receptor tandem BAM1/BAM2 regulates epidermal cell division homeostasis. Consequently, HSL1-IDLs and BAM1/BAM2-CLEs independently regulate cell patterning in the leaf epidermal tissue.

UR - http://www.scopus.com/inward/record.url?scp=85124680110&partnerID=8YFLogxK

U2 - 10.1038/s41467-022-28558-4

DO - 10.1038/s41467-022-28558-4

M3 - Article

C2 - 35169143

AN - SCOPUS:85124680110

VL - 13

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 876

ER -