The transcription factor ESR2/DRNL/BOL differentially regulates de novo organogenesis, regeneration, and lateral root development in Arabidopsis thaliana

Abstract

Plant regeneration requires coordinated transcriptional and hormonal regulation to re-establish organ identity. The AP2/ERF transcription factor ENHANCER OF SHOOT REGENERATION 2 /DORNROESCHEN-LIKE / BOLITA (ESR2/DRNL/BOL) expressed in aerial organ founder cells promotes shoot formation, but its broader role across organogenic contexts remains unclear. Here, using loss-of-function and inducible overexpression lines of Arabidopsis thaliana, we demonstrate that ESR2 exerts context-dependent and antagonistic effects on shoot and root development. ESR2 activation promotes shoot and aerial-like tissue formation and enhances callus proliferation, particularly under cytokinin-rich conditions. Conversely, ESR2 suppresses or delays multiple de novo root formation programs, including adventitious, basal, and regenerated roots, while its loss enhances root initiation and growth. Expression analyses reveal that ESR2 promoter activity is found at de novo formed basal and adventitious root primordia and emerged root apical meristems, suggesting a role in conferring regenerative competence while restricting their developmental progression. Moreover, it is expressed in newly established quiescent centers of lateral roots in intact plants and the loss of ESR2 function strongly and negatively affects lateral root initiation, revealing an unanticipated developmental role of ESR2 and its requirement for lateral root formation. Together, these findings identify ESR2 as a shared molecular regulator governing early organogenesis in intact plants and plant explants; it establishes an aerial organ fate bias while maintaining the competence for -and limiting the progression of- de novo root development in explants.