SCREAM promotes the timely termination of proliferative divisions in stomatal lineage by directly suppressing...

Stomata are produced through a series of asymmetric cell divisions (ACDs) and one symmetric division. In the Arabidopsis stomatal lineage, the number of ACDs in meristemoids is strictly limited to 1-3 rounds before meristemoids differentiate into guard mother cells. However, the precise regulatory mechanisms that govern this pattern formation remain largely elusive. Here, we identify a unique mechanism of SCREAM (SCRM) in terminating proliferative ACDs of meristemoids by directly suppressing SPEECHLESS (SPCH), a master initiator of stomatal ACDs. The mutation of SCRM, rather than SCRM2, results in a delayed proliferation-to-differentiation transition, as well as an excessive phenotype of ACDs. Conversely, overexpression of SCRM promotes the timely termination of proliferative divisions. Expression of stomatal-linage marker genes is upregulated in scrm and downregulated in SCRM_OE plants. Multiple assays have demonstrated that SCRM, activated by SPCH, directly binds to the promoter of SPCH and represses its expression. Genetic analysis supports that SCRM acts upstream of SPCH, thus forming a loop of SPCH-SCRM-SPCH to maintain the balance between the initiation and termination of ACDs. Our findings reveal a distinct role of SCRM in regulating proliferative divisions and provide insight into the mechanism governing the limited rounds of ACDs in meristemoids.