Shoot-borne adventitious/crown roots form a highly derived fibrous root system in grasses. The molecular mechanisms controlling their development remain largely unknown. Here, we provide a genome-wide landscape of transcriptional signatures – tightly regulated auxin response and in-depth spatio-temporal expression patterns of potential epigenetic modifiers – and transcription factors during priming and outgrowth of rice (Oryza sativa) crown root primordia. Functional analyses of rice transcription factors from WUSCHEL-RELATED HOMEOBOX and PLETHORA gene families reveal their non-redundant and species-specific roles in determining the root architecture. WOX10 and PLT1 regulate both shoot-borne crown roots and root-borne lateral roots, but PLT2 specifically controls lateral root development. PLT1 activates local auxin biosynthesis genes to promote crown root development. Interestingly, O. sativa PLT genes rescue lateral root primordia outgrowth defects of Arabidopsis plt mutants, demonstrating their conserved role in root primordia outgrowth irrespective of their developmental origin. Together, our findings unveil a molecular framework of tissue transdifferentiation during root primordia establishment, leading to the culmination of robust fibrous root architecture. This also suggests that conserved factors have evolved their transcription regulation to acquire species-specific function.