Phosphate (P) deficiency severely limits the growth and production of plants. Adventitious root development plays an essential role in responding to low phosphorus stress for apple plants. However, the molecular mechanisms regulating adventitious root growth and development in response to low phosphorus stress have remained elusive. In this study, a mutation (C-T) in the coding region of the apple AUXIN/INDOLE-3-ACETIC ACID 27 (IAA27) gene was identified. MdIAA27T-overexpressing transgenic apple improved the tolerance to phosphorus deficiency, which grew longer and denser adventitious roots and presented higher phosphorous content than the control plants under low phosphorus conditions, while the overexpression of MdIAA27C displayed the opposite trend. Moreover, the heterologous overexpression of MdIAA27 in tobacco yielded the same results, supporting the aforementioned findings. In vitro and in vivo assays showed that MdIAA27 directly interacted with AUXIN RESPONSE FACTOR (ARF8), ARF26 and ARF27, which regulated Small Auxin-Up RNA 76 (MdSAUR76) and lateral organ boundaries domain 16 (MdLBD16) transcription. The mutation in IAA27 resulted in altered interaction modes, which in turn promoted the release of positive ARFs to upregulate SAUR76 and LBD16 expression in low phosphorus conditions. Altogether, our studies provide insights into how the allelic variation of IAA27 affects adventitious root development in response to low phosphorus stress.

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