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Receptor kinases <i>DRUS1</i> (<i>Dwarf and Runtish Spikelet1</i>) and <i>DRUS2</i> are orthologues of the renowned <i>Arabidopsis thaliana</i> gene <i>FERONIA</i>, which play redundant roles in rice growth and development. Whether the two duplicated genes perform distinct functions in response to environmental stress is largely unknown. Here, we found that osmotic stress (OS) and ABA increased <i>DRUS1</i> expression while decreasing <i>DRUS2</i>. When subjected to osmotic stress, the increased <i>DRUS1</i> in <i>drus2</i> mutants suppresses the <i>OsIAA</i> repressors, resulting in a robust root system with an increased number of adventitious and lateral roots as well as elongated primary, adventitious, and lateral roots, conferring OS tolerance. In contrast, the decreased <i>DRUS2</i> in <i>drus1-1</i> mutants are not sufficient to suppress <i>OsIAA</i> repressors, leading to a feeble root system with fewer adventitious and lateral roots and hindering seminal root growth, rendering OS intolerance. All these findings offer valuable insights into the biological significance of the duplication of two homologous genes in rice, wherein, if one is impaired, the other one is able to continue auxin-signaling-mediated root growth and development to favor resilience to environmental stress, such as water shortage.