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The development of above-ground lateral organs is initiated at the peripheral zone of the shoot apical meristem (SAM). The coordination of cell fate determination and the maintenance of stem cells are achieved through a complex regulatory network comprised of transcription factors. Two AP2/ERF transcription factor family genes, <i>ESR1/DRN</i> and <i>ESR2/DRNL/SOB/BOL</i>, regulate cotyledon and flower formation and de novo organogenesis in tissue culture. However, their roles in post-embryonic lateral organ development remain elusive. In this study, we analyzed the genetic interactions among SAM-related genes, <i>WUS</i> and <i>STM</i>, two <i>ESR</i> genes, and one of the HD-ZIP III members, <i>REV</i>, whose protein product interacts with ESR1 in planta. We found that <i>esr1</i> mutations substantially enhanced the <i>wus</i> and <i>stm</i> phenotypes, which bear a striking resemblance to those of the <i>wus rev</i> and <i>stm rev</i> double mutants, respectively. Aberrant adaxial–abaxial polarity is observed in <i>wus</i> <i>esr1</i> at relatively low penetrance. On the contrary, the <i>esr2</i> mutation partially suppressed <i>stm</i> phenotypes in the later vegetative phase. Such complex genetic interactions appear to be attributed to the distinct expression pattern of two <i>ESR</i> genes because the <i>ESR1</i> promoter-driving <i>ESR2</i> is capable of rescuing phenotypes caused by the <i>esr1</i> mutation. Our results pose the unique genetic relevance of <i>ESR1</i> and the SAM-related gene interactions in the development of rosette leaves.