Fine control of aerenchyma and lateral root development through AUX/IAA- and ARF-dependent auxin signaling

Abstract

Lateral roots (LRs) are derived from a parental root and contribute to water and nutrient uptake from the soil. Auxin/indole-3-acetic acid protein (AUX/IAA; IAA) and auxin response factor (ARF)-mediated signaling are essential for LR formation. Lysigenous aerenchyma, a gas space created by cortical cell death, aids internal oxygen transport within plants. Rice (Oryza sativa) forms lysigenous aerenchyma constitutively under aerobic conditions and increases its formation under oxygen-deficient conditions; however, the molecular mechanisms regulating constitutive aerenchyma (CA) formation remain unclear. LR number is reduced by the dominant-negative effect of a mutated AUX/IAA protein in the iaa13 mutant. We found that CA formation is also reduced in iaa13 We have identified ARF19 as an interactor of IAA13 and identified a lateral organ boundary domain (LBD)-containing protein (LBD1-8) as a target of ARF19. IAA13, ARF19, and LBD1-8 were highly expressed in the cortex and LR primordia, suggesting that these genes function in the initiation of CA and LR formation. Restoration of LBD1-8 expression recovered aerenchyma formation and partly recovered LR formation in the iaa13 background, in which LBD1-8 expression was reduced. An auxin transport inhibitor suppressed CA and LR formation, and a natural auxin stimulated CA formation in the presence of the auxin transport inhibitor. Our findings suggest that CA and LR formation are both regulated through AUX/IAA- and ARF-dependent auxin signaling. The initiation of CA formation lagged that of LR formation, which indicates that the formation of CA and LR are regulated differently by auxin signaling during root development in rice.