Reactive oxygen species and reactive carbonyl species constitute a feed‐forward loop in auxin signaling for lateral root formation

Biswas, Md. Sanaullah; Fukaki, Hidehiro; Mori, Izumi C.; Nakahara, Kazuha; Mano, Junichi

doi:10.1111/tpj.14456

Cited by 63 publications

(61 citation statements)

References 71 publications

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“…Despite the understanding that auxin induces ROS production to regulate cell elongation (Schopfer, 2001) and root gravitropism (Joo et al, 2001), the molecular relationship between ROS and auxin remains largely unknown. Recent study revealed the potential feed-forward loop between ROS and auxin signaling to control lateral root formation (Biswas et al, 2019). It was confirmed that production of reactive oxygen species (ROS) via the hormone-induced activation of respiratory burst oxidase homologous NADPH oxidases facilitates lateral root (LR) formation, and that the auxin-induced production of ROS and their downstream products RCS (reactive carbonyl species) modulate the auxin signaling pathway in a feed-forward manner.…”

Section: Ros Interact With Other Signaling Hormones To Regulate Root mentioning

confidence: 93%

“…•− and H 2 O 2 accumulate in the meristematic and elongation zones, respectively (Dunand et al, 2007;Biswas et al, 2019). An imbalance will lead to a change in the size of the meristematic zone.…”

Section: Gradient Distribution Of Ros Regulates Root Stem Cell Differmentioning

confidence: 99%

“…It was confirmed that production of reactive oxygen species (ROS) via the hormone-induced activation of respiratory burst oxidase homologous NADPH oxidases facilitates lateral root (LR) formation, and that the auxin-induced production of ROS and their downstream products RCS (reactive carbonyl species) modulate the auxin signaling pathway in a feed-forward manner. RCS are key agents that connect the ROS signaling and the auxin signaling pathways (Biswas et al, 2019).…”

Section: Ros Interact With Other Signaling Hormones To Regulate Root mentioning

confidence: 99%

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

Zhou

et al. 2020

Front. Plant Sci.

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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

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Section: Ros Interact With Other Signaling Hormones To Regulate Root mentioning

confidence: 93%

Section: Gradient Distribution Of Ros Regulates Root Stem Cell Differmentioning

confidence: 99%

Section: Ros Interact With Other Signaling Hormones To Regulate Root mentioning

confidence: 99%

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

Zhou

et al. 2020

Front. Plant Sci.

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“…RCS is a group name of the α,β-unsaturated aldehydes and ketones, such as acrolein and 4-hydroxy-(E)-2-nonenal (HNE) [13,14]. RCS are generated from lipid peroxides (LOOH) and act as agents to mediate ROS signal to target proteins in the heat shock-responsive gene regulation [15], senescence [16], abscisic acid (ABA) signaling for stomatal closure [17,18], and auxin signaling for lateral root formation [19] in plants. We reported that tobacco BY-2 cells exposed to H 2 O 2 generated acrolein and HNE, and a chemical carbonyl scavenger prevented the initiation of PCD, without affecting the increase in the intracellular ROS level [12].…”

Section: Introductionmentioning

confidence: 99%

Inactivation of Carbonyl-Detoxifying Enzymes by H2O2 Is a Trigger to Increase Carbonyl Load for Initiating Programmed Cell Death in Plants

2020

Self Cite

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H2O2-induced programmed cell death (PCD) of tobacco Bright Yellow-2 (BY-2) cells is mediated by reactive carbonyl species (RCS), degradation products of lipid peroxides, which activate caspase-3-like protease (C3LP). Here, we investigated the mechanism of RCS accumulation in the H2O2-induced PCD of BY-2 cells. The following biochemical changes were observed in 10-min response to a lethal dose (1.0 mM) of H2O2, but they did not occur in a sublethal dose (0.5 mM) of H2O2. (1) The C3LP activity was increased twofold. (2) The intracellular levels of RCS, i.e., 4-hydroxy-(E)-hexenal and 4-hydroxy-(E)-nonenal (HNE), were increased 1.2–1.5-fold. (3) The activity of a reduced nicotinamide adenine dinucleotide phosphate (NADPH)-dependent carbonyl reductase, scavenging HNE, and n-hexanal was decreased. Specifically, these are the earliest events leading to PCD. The proteasome inhibitor MG132 suppressed the H2O2-induced PCD, indicating that the C3LP activity of the β1 subunit of the 20S proteasome was responsible for PCD. The addition of H2O2 to cell-free protein extract inactivated the carbonyl reductase. Taken together, these results suggest a PCD-triggering mechanism in which H2O2 first inactivates a carbonyl reductase(s), allowing RCS levels to rise, and eventually leads to the activation of the C3LP activity of 20S proteasome. The carbonyl reductase thus acts as an ROS sensor for triggering PCD.

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“…In order to maintain normal growth under adverse conditions, plants must be able to readily remove ROS, preventing the damage to cellular components and cellular structures (Biswas et al 2019). In S. salsa, the photochemistry in photosystem II did not change when the plants were grown under high-salinity conditions (100-400 mM NaCl), indicating that high salinity did not affect the photosynthetic apparatus (Lu et al 2002).…”

Section: Regulation Of Antioxidant Levels During Seedling Growthmentioning

confidence: 99%

Adaptation of the Euhalophyte Suaeda salsa to High-Salinity Conditions

Guo¹,

Song²,

Wang³

2020

Handbook of Halophytes

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Halophytes can complete their lifecycles in natural environments with high levels of salt (200 mM NaCl or more). Therefore, halophytes represent excellent sources of salt-tolerant genes for use in traditional crops to improve the efficiency of agriculture in saline-alkali environments. Here, we review the latest information about Suaeda salsa, an especially promising genetic resource. This typical euhalophyte has succulent leaves and grows in saline habitats in inland and intertidal zones. S. salsa produces dimorphic seeds (black and brown seeds) on the same plant under natural growth conditions. These seeds have different J.G and J.S. wrote the paper; B.W. revised the paper.

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Reactive oxygen species and reactive carbonyl species constitute a feed‐forward loop in auxin signaling for lateral root formation

Cited by 63 publications

References 71 publications

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

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

Inactivation of Carbonyl-Detoxifying Enzymes by H2O2 Is a Trigger to Increase Carbonyl Load for Initiating Programmed Cell Death in Plants

Adaptation of the Euhalophyte Suaeda salsa to High-Salinity Conditions

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