Coordinated spacing and patterning of stomata allow efficient gas exchange between plants and the atmosphere. Here we report that three ERECTA (ER)-family leucine-rich repeat-receptor-like kinases (LRR-RLKs) together control stomatal patterning, with specific family members regulating the specification of stomatal stem cell fate and the differentiation of guard cells. Loss-of-function mutations in all three ER-family genes cause stomatal clustering. Genetic interactions with a known stomatal patterning mutant too many mouths (tmm) revealed stoichiometric epistasis and combination-specific neomorphism. Our findings suggest that the negative regulation of ER-family RLKs by TMM, which is an LRR receptor-like protein, is critical for proper stomatal differentiation.

Growth of plant organs relies on coordinated cell proliferation followed by cell growth, but the nature of the cell-cell signal that specifies organ size remains elusive. The Arabidopsis receptor-like kinase (RLK) ERECTA regulates inflorescence architecture. Our previous study using a dominant-negative fragment of ERECTA revealed the presence of redundancy in the ERECTA-mediated signal transduction pathway. Here, we report that Arabidopsis ERL1 and ERL2, two functional paralogs of ERECTA, play redundant but unique roles in a part of the ERECTA signaling pathway, and that synergistic interaction of three ERECTA-family RLKs define aerial organ size. Although erl1 and erl2 mutations conferred no detectable phenotype, they enhanced erecta defects in a unique manner. Overlapping but distinct roles of ERL1 and ERL2 can be ascribed largely to their intricate expression patterns rather than their functions as receptor kinases. Loss of the entire ERECTA family genes led to striking dwarfism, reduced lateral organ size and abnormal flower development,including defects in petal polar expansion, carpel elongation, and anther and ovule differentiation. These defects are due to severely reduced cell proliferation. Our findings place ERECTA-family RLKs as redundant receptors that link cell proliferation to organ growth and patterning.

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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.