Modulatory Role of Reactive Oxygen Species in Root Development in Model Plant of Arabidopsis thaliana

Abstract

Reactive oxygen species (ROS), a type of oxygen monoelectronic reduction product, have a higher chemical activity than O 2. Although ROS pose potential risks to all organisms via inducing oxidative stress, indispensable role of ROS in individual development cannot be ignored. Among them, the role of ROS in the model plant Arabidopsis thaliana is deeply studied. Mounting evidence suggests that ROS are essential for root and root hair development. In the present review, we provide an updated perspective on the latest research progress pertaining to the role of ROS in the precise regulation of root stem cell maintenance and differentiation, redox regulation of the cell cycle, and root hair initiation during root growth. Among the different types of ROS, O 2 •− and H 2 O 2 have been extensively investigated, and they exhibit different gradient distributions in the roots. The concentration of O 2 •− decreases along a gradient from the meristem to the transition zone and the concentration of H 2 O 2 decreases along a gradient from the differentiation zone to the elongation zone. These gradients are regulated by peroxidases, which are modulated by the UPBEAT1 (UPB1) transcription factor. In addition, multiple transcriptional factors, such as APP1, ABO8, PHB3, and RITF1, which are involved in the brassinolide signaling pathway, converge as a ROS signal to regulate root stem cell maintenance. Furthermore, superoxide anions (O 2 •−) are generated from the oxidation in mitochondria, ROS produced during plasmid metabolism, H 2 O 2 produced in apoplasts, and catalysis of respiratory burst oxidase homolog (RBOH) in the cell membrane. Furthermore, ROS can act as a signal to regulate redox status, which regulates the expression of the cell-cycle components CYC2;3, CYCB1;1, and retinoblastoma-related protein, thereby controlling the cell-cycle progression. In the root maturation zone, the epidermal cells located in the H cell position emerge to form hair cells, and plant hormones, such as auxin and ethylene regulate root hair formation via ROS. Furthermore, ROS accumulation can influence hormone signal transduction and vice versa. Data about the association between nutrient stress and ROS signals in root hair development are scarce. However, the fact that ROBHC/RHD2 or RHD6 is specifically expressed in root hair cells and induced by nutrients, may explain the relationship. Future studies should focus on the regulatory

The TOR–Auxin Connection Upstream of Root Hair Growth

“…ROS signaling is a fundamental regulatory element of plant growth, including the fine-tuning of tropistic reactions via auxin flow regulation [ 8 , 144 , 155 , 156 ]. ROS produced by NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE-OXIDASE(NOX) is needed to stimulate root hair elongation [ 150 , 157 , 158 ]. Furthermore, ROS accumulation is crucial for root hair tip outgrowth by modulating cell wall properties [ 152 ], regulating the rearrangement and abundance of the secondary messenger, cytoskeleton arrangement, and PM remodeling [ 150 , 159 , 160 ], and pH changes in the apoplast upon auxin efflux [ 8 ].…”

“…ROS produced by NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE-OXIDASE(NOX) is needed to stimulate root hair elongation [ 150 , 157 , 158 ]. Furthermore, ROS accumulation is crucial for root hair tip outgrowth by modulating cell wall properties [ 152 ], regulating the rearrangement and abundance of the secondary messenger, cytoskeleton arrangement, and PM remodeling [ 150 , 159 , 160 ], and pH changes in the apoplast upon auxin efflux [ 8 ]. The calcium gradient at the root hair tip controls the direction of growth, and Ca 2+ is a universal second messenger, crucial to modulate developmental plasticity in plants [ 8 ].…”

“…This triggers changes in the PM composition [ 171 ], resulting in the differential bundling of microtubules and actin at the root hair tip [ 172 , 173 ]. ROP2 activates ROS generation through NADPH oxidase action [ 150 , 166 , 174 ]. Plants overexpressing ROP2 have longer hairs than wild-type plants [ 69 ] and multiple root hair outgrowths per trichoblast [ 175 ] suggest that its function is needed during all stages of root hair growth.…”

Temperature-dependent fasciation mutants provide a link between mitochondrial RNA processing and lateral root morphogenesis

“…•promotes cell proliferation in the meristematic zone, while H 2 O 2 induces cell differentiation in the elongation zone (Tsukagoshi et al, 2010;Zhou et al, 2020). The transcription factor UPBEAT1 (UPB1) is suggested to regulate the transition between the two zones, via the suppression of extracellular peroxidase activity in the elongation zone (Tsukagoshi et al, 2010;Zhou et al, 2020).…”

“…•promotes cell proliferation in the meristematic zone, while H 2 O 2 induces cell differentiation in the elongation zone (Tsukagoshi et al, 2010;Zhou et al, 2020). The transcription factor UPBEAT1 (UPB1) is suggested to regulate the transition between the two zones, via the suppression of extracellular peroxidase activity in the elongation zone (Tsukagoshi et al, 2010;Zhou et al, 2020). Interestingly, during LR formation, factors involved in apoplastic ROS regulation, UPB1 and another transcription factor MYB36, as well as some members of the RESPIRATORY BURST OXIDASE HOMOLOG (RBOH) family, are expressed in the periphery of the LR primordium (Fernández-Marcos et al, 2017;Manzano et al, 2014;Orman-Ligeza et al, 2016); however, the role of apoplastic ROS in controlling the proliferation-to-differentiation transition in the LR boundary remains largely speculative.…”