OsPIN1b, OsPIN1c, and OsPIN9 mediate shoot-to-root auxin transport to activate cutting-induced compensatory root growth

Plant roots are often severed during transplanting, but plants can recover from partial root loss through compensatory growth. However, the mechanisms regulating this compensatory growth are not fully understood. Here, we showed that cutting rice (Oryza sativa L.) seminal roots induces high auxin accumulation around the incision site. This auxin accumulation enhanced the expression of the transcription factor WUSCHEL-RELATED HOMEOBOX10 (OsWOX10) and promoted lateral root (LR) primordia development into long and thick L-type LRs, thus compensating for the partial loss of seminal roots. Removing the coleoptile or blocking shoot-to-root auxin transport inhibited auxin accumulation around the incision site and abolished compensatory LR growth. Three auxin efflux proteins, OsPIN1b, OsPIN1c, and OsPIN9, are expressed in the root vasculature and epidermis in the root tip meristem zone, and redundantly control shoot-to-root auxin transport and root tip auxin distribution. Knocking out all 3 PIN genes caused severe growth inhibition and loss of gravitropism, as well as diminished cutting-induced auxin accumulation and compensatory LR growth, whereas knockout of 1 or 2 genes had little effect. Soil transplanting experiments showed that weakened compensatory LR growth hinders plant growth and nutrient absorption after cutting. Jasmonic acid, reactive oxygen species, and cytosolic calcium signaling, which are important for wounding responses, were not involved in compensatory LR growth. Our study reveals that OsPIN1b, OsPIN1c, and OsPIN9 mediate shoot-to-root auxin transport, and that auxin accumulation around the incision site triggers compensatory LR growth after physical damage to rice roots.