A receptor-like protein acts as a specificity switch for the regulation of stomatal development

Abstract

Stomata are microscopic openings that allow for the exchange of gases between plants and the environment. In , stomatal patterning is specified by the ERECTA family (ERf) receptor kinases (RKs), the receptor-like protein (RLP) TOO MANY MOUTHS (TMM), and EPIDERMAL PATTERNING FACTOR (EPF) peptides. Here we show that TMM and ER or ER-LIKE1 (ERL1) form constitutive complexes, which recognize EPF1 and EPF2, but the single ERfs do not. TMM interaction with ERL1 creates a binding pocket for recognition of EPF1 and EPF2, indicating that the constitutive TMM-ERf complexes function as the receptors of EPF1 and EPF2. EPFL9 competes with EPF1 and EPF2 for binding to the ERf-TMM complex. EPFL4 and EPFL6, however, are recognized by the single ERfs without the requirement of TMM. In contrast to EPF1,2, the interaction of EPFL4,6 with an ERf is greatly reduced in the presence of TMM. Taken together, our data demonstrate that TMM dictates the specificity of ERfs for the perception of different EPFs, thus functioning as a specificity switch for the regulation of the activities of ERfs.

Constitutive activation of leucine-rich repeat receptor kinase signaling pathways by BAK1-interacting receptor-like kinase 3 chimera

“…SERK proteins have been previously shown to allow for receptor activation of ERECTA family receptor kinases in protoderm formation and stomatal patterning (Meng et al, 2015). ER forms constitutive complexes with the LRR-RLP TMM to sense EPF peptides in stomatal patterning (Yang and Sack, 1995;Nadeau and Sack, 2002;Lee et al, 2012Lee et al, , 2015Lin et al, 2017), but it is not understood at the mechanistic level how SERK co-receptor kinases allow for receptor activation of this LRR-RK/LRR-RLP signaling complex (Lin et al, 2017). To test if the receptor activation mechanism is conserved among BRI1, HAESA and ER, we expressed a chimeric oBIR3-iER construct fused to a C-terminal yellow fluorescent protein YPET specifically in the stomata lineage under control of the meristemoid-specific MUTE promoter ( Figure 4A) (Pillitteri et al, 2007).…”

“…LRR-RKs form the largest class of receptor kinases known in plants (Shiu and Bleecker, 2001). Members of the family have been shown to sense small molecule (Wang et al, 2001), peptide (Gómez-Gómez and Boller, 2000;Matsubayashi, 2014;Santiago et al, 2016) and protein ligands (Huang et al, 2016;Lin et al, 2017;Zhang et al, 2017).…”

“…The plant-unique SERK co-receptor dependent activation mechanism is conserved among many LRR-RKs (Hohmann et al, 2017), including the LRR-RK HAESA, which, for example, controls floral organ abscission in Arabidopsis by interacting with the peptide hormone IDA (Jinn et al, 2000;Meng et al, 2016;Santiago et al, 2016;Hohmann et al, 2018b). A SERK-dependent (Yang and Sack, 1995;Nadeau and Sack, 2002;Lee et al, 2012Lee et al, , 2015Lin et al, 2017). EPF peptide binding to these LRR-RK/LRR-RLP complexes triggers their interaction with SERK coreceptor kinases (Meng et al, 2015;Lin et al, 2017), which in turn leads to the initiation of a MAP kinase signaling pathway that includes the MAP3K YODA (Bergmann et al, 2004).…”

“…A SERK-dependent (Yang and Sack, 1995;Nadeau and Sack, 2002;Lee et al, 2012Lee et al, , 2015Lin et al, 2017). EPF peptide binding to these LRR-RK/LRR-RLP complexes triggers their interaction with SERK coreceptor kinases (Meng et al, 2015;Lin et al, 2017), which in turn leads to the initiation of a MAP kinase signaling pathway that includes the MAP3K YODA (Bergmann et al, 2004). Stimulation of the ERECTA pathway negatively regulates stomata formation (Lampard et al, 2009).…”

“…Complex structures and quantitative biochemical comparisons of different ligand-activated LRR-RK -SERK complexes have revealed a structurally and functionally conserved activation mechanism, relying on the interaction of the ligand bound receptor LRR ectodomain with the shape-complementary ectodomain of the SERK co-receptor (Santiago et al, 2013;Wang et al, 2015;Santiago et al, 2016;Hohmann et al, 2017;Lin et al, 2017;Hohmann et al, 2018b). The ligand binding specificity of plant LRR-RKs is encoded in their LRR ectodomains (Hohmann et al, 2017;Okuda et al, 2020).…”