Enhanced root hair production, which increases the root surface area for nutrient uptake, is a typical adaptive response of plants to
phosphate (Pi)
starvation. Although previous studies have shown that
ethylene plays an important role in root hair development induced by Pi
starvation, the underlying molecular mechanism is not understood. In this work, we characterized an Arabidopsis mutant, hps5, that displays constitutive
ethylene responses and increased sensitivity to Pi
starvation due to a mutation in the
ethylene receptor ERS1. hps5 accumulates high levels of EIN3
protein, a key
transcription factor involved in the
ethylene signaling pathway, under both Pi sufficiency and deficiency. Pi
starvation also increases the accumulation of EIN3
protein. Combined molecular, genetic, and genomic analyses identified a group of genes that affect root hair development by regulating cell wall modifications. The expression of these genes is induced by Pi
starvation and is enhanced in the EIN3-overexpressing line. In contrast, the induction of these genes by Pi
starvation is suppressed in ein3 and ein3eil1 mutants. EIN3
protein can directly bind to the promoter of these genes, some of which are also the immediate targets of RSL4, a key
transcription factor that regulates root hair development. Based on these results, we propose that under normal growth conditions, the level of
ethylene is low in root cells; a group of key
transcription factors, including RSL4 and its homologs, trigger the transcription of their target genes to promote root hair development; Pi
starvation increases the levels of the
protein EIN3, which directly binds to the promoters of the genes targeted by RSL4 and its homologs and further increase their transcription, resulting in the enhanced production of root hairs. This model not only explains how
ethylene mediates root hair responses to Pi
starvation, but may provide a general mechanism for how
ethylene regulates root hair development under both stress and non-stress conditions.