Rice adventitious/crown roots developing from non-root tissues shape up the root architecture.Mechanisms underlying initiation and subsequent outgrowth of CR primordia (CRP) remain under explored. Here, we provide genome-wide dynamics of gene expression patterns and stage-specific transcriptional signatures at distinct developmental stages of CRP formation. Our analyses reveal that early regulated transcription of potential epigenetic modifiers, transcription factors and cell division regulators prime the initiation of CRP followed by progressive activation of auxin signaling modules ensure their outgrowth. In depth analysis of spatio-temporal expression patterns of key cell fate determinants and functional analyses of rice WUSCHEL RELATED HOMEOBOX10 (OsWOX10) and PLETHORA (OsPLT) genes reveal their unprecedented role in CRP development. Our study suggests that OsWOX10 activates OsERF3 and OsCRL1 expression during CRP initiation and OsPLTs expression to accomplish their outgrowth. Interestingly, OsPLT genes, when expressed in the transcriptional domain of root-borne lateral root primordia of Arabidopsis plt mutant, rescued their outgrowth demonstrating the conserved role of PLT genes in root primordia outgrowth irrespective of their developmental origin. Together, these findings unveil the molecular framework of cellular reprogramming during trans-differentiation of shoot tissue to root leading to culmination of robust root architecture in monocot species which got evolutionary diverged from dicots. T.G. performed experiments of LCM, RNA in situ hybridization and OsWOX10 function in rice. Z.S. performed experiments for auxin responses and functions of OsPLT1 and OsPLT4 in rice. A.K.D., R.S.S and M.J. performed RNA sequencing data analysis. M.Y. with T.G. contributed for function of OsWOX10 in Arabidopsis. V.V. studied function of rice PLTs in Arabidopsis. D.C. contributed in LCM experiments. M.J., K.P. and S.R.Y. designed experiments, analyzed data and Academy of Sciences, Shanghai, China is acknowledged for kindly providing Arabidopsis wox11-2, wox12-1 and wox11-2 wox12-1 seeds. Ashish Kumar and Sonia Choudhary are acknowledged for their support in growing plants.