Flavonols regulate root hair development by modulating accumulation of reactive oxygen species in the root epidermis

Abstract

Reactive oxygen species (ROS) are signaling molecules produced by tissue-specific respiratory burst oxidase homolog (RBOH) enzymes to drive development. In Arabidopsis thaliana, ROS produced by RBOHC was previously reported to drive root hair elongation. We identified a specific role for one ROS, H 2 O 2 , in driving root hair initiation and demonstrated that localized synthesis of flavonol antioxidants control the level of H 2 O 2 and root hair formation. Root hairs form from trichoblast cells that express RBOHC and have elevated H 2 O 2 compared with adjacent atrichoblast cells that do not form root hairs. The flavonol-deficient tt4 mutant has elevated ROS in trichoblasts and elevated frequency of root hair formation compared with the wild type. The increases in ROS and root hairs in tt4 are reversed by genetic or chemical complementation. Auxin-induced root hair initiation and ROS accumulation were reduced in an rbohc mutant and increased in tt4, consistent with flavonols modulating ROS and auxin transport. These results support a model in which localized synthesis of RBOHC and flavonol antioxidants establish patterns of ROS accumulation that drive root hair formation.

Flavonols modulate lateral root emergence by scavenging reactive oxygen species inArabidopsis thaliana

“…Arabidopsis mutants with defects in flavonol synthesis have elevated levels of auxin transport, consistent with the absence of a negative regulator of auxin transport (11,16,17). Consistent with the antioxidant capabilities of flavonols, mutants that have impaired flavonol biosynthesis have higher levels of ROS in guard cells, root hairs, and pollen tubes (9,10,14,15).…”

“…Flavonols are a subclass of flavonoid specialized metabolites that function as antioxidants in plants and regulate developmental and stress responses (2,9,15). Arabidopsis produces three flavonols, kaempferol, quercetin, and isorhamnetin (2,63), which can be further modified via glycosylation, leading to a set of molecules with different antioxidant capabilities and distinct functions in vivo (5,9,13). The tt4(2YY6) and tt4-1 mutants, which produce no flavonols, were previously reported to have increased numbers of lateral roots (18,19).…”

“…Our results better support the hypothesis that the function of flavonol metabolites is to scavenge ROS that modulates lateral root development. Flavonol compounds have been shown to act as antioxidants in vivo to modulate stomatal aperture (10,14), pollen viability (15), and root hair number (9). To ask if the developmental effects of flavonol mutants were tied to the ROS status, we treated roots with ascorbic acid.…”

“…The upregulation of flavonol biosynthesis is well described in response to environmental stress, hormones, and development signals (2,9,10,14,15). Additionally, flavonoid precursors can be transported both short and long distances (58,59), which could implicate a role for flavonols in long distance signaling.…”

“…The low baseline levels of ROS allow local increases in ROS to act as important developmental signals. In Arabidopsis, ROS signaling has been implicated in stomatal closure (10,14,34,35), pollen tube growth and development (15,(36)(37)(38), root hair elongation (9,39), root gravitropism and phototropism (40)(41)(42), primary root elongation (43), the transition from cell proliferation to elongation in the root tip (44), and lateral root emergence (20)(21)(22). ROS signaling is also involved in the production of the casparian strip (45), and resistance to stress including hypoxia, salt stress, and ozone (46)(47)(48).…”