The Molecular Link Between Auxin And ROS-Mediated Polar Growth
Silvina Mangano2017
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Abstract
Root hair polar growth is endogenously controlled by auxin and sustained by oscillating levels of reactive oxygen species (ROS). These cells extend several hundred-fold their original size toward signals important for plant survival. Although their final cell size is of fundamental importance, the molecular mechanisms that control it remain largely unknown. Here, we show that ROS production is controlled by the transcription factors RSL4, which in turn is transcriptionally regulated by auxin through several Auxin Responsive Factors (ARFs). In this manner, auxin controls ROS-mediated polar growth by activating RSL4, which then upregulates the expression of genes encoding NADPH oxidases (also known as RBOHs, RESPIRATORY BURST OXIDASE HOMOLOG proteins) and Class-III Peroxidases (PER), which catalyse ROS production. Chemical or genetic interference with the ROS balance or peroxidase activity affect root hair final cell size. Overall, our findings establish a molecular link between auxin...
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Title: The molecular link between auxin and ROS-mediated polar root hair growth Authors for Correspondence
2017
Root hair polar growth is endogenously controlled by auxin and sustained by oscillating levels of reactive oxygen species (ROS). These cells extend several hundred-fold their original size toward signals important for plant survival. Although their final cell size is of fundamental importance, the molecular mechanisms that control it remain largely unknown. Here, we show that ROS production is controlled by the transcription factors RSL4, which in turn is transcriptionally regulated by auxin through several Auxin Responsive Factors (ARFs). In this manner, auxin controls ROS-mediated polar growth by activating RSL4, which then upregulates the expression of genes encoding NADPH oxidases (also known as RBOHs, RESPIRATORY BURST OXIDASE HOMOLOG proteins) and Class-III Peroxidases (PER), which catalyse ROS production. Chemical or genetic interference with the ROS balance or peroxidase activity affect root hair final cell size. Overall, our findings establish a molecular link between auxin regulated ARFs-RSL4 and ROS-mediated polar root hair growth. Significance Statement Tip-growing root hairs are excellent model systems to decipher the molecular mechanism underlying reactive oxygen species (ROS)-mediated cell elongation. Root hairs are able to expand in response to external signals, increasing several hundred-fold their original size, which is important for survival of the plant. Although their final cell size is of fundamental importance, the molecular mechanisms that control it remain largely unknown. In this study, we propose a molecular mechanism that links the auxin-Auxin Response Factors (ARFs) module to activation of RSL4, which directly targets genes encoding ROSproducing enzymes, such as NADPH oxidases (or RBOHs) and secreted type-III peroxidases (PERs). Activation of these genes impacts apoplastic ROS homeostasis, thereby stimulating root hair cell elongation.
High Auxin and High Phosphate Impact on RSL2 Expression and ROS-Homeostasis Linked to Root Hair Growth in Arabidopsis thaliana
Frontiers in Plant Science
Root hair size determines the surface area/volume ratio of the whole roots exposed to the nutrient and water pools, thereby likely impacting nutrient and water uptake rates. The speed at which they grow is determined both by cell-intrinsic factors like hormones (e.g., auxin) and external environmental signals like nutrient availability in the soil (e.g., phosphate). Overall root hair growth is controlled by the transcription factors RSL4 and RSL2. While high levels of auxin promote root hair growth, high levels of inorganic phosphate (Pi) in the media are able to strongly repress RSL4 and RSL2 expression linked to a decreased polar growth. In this work, we inquired the mechanism used by root hairs to integrate conflicting growth signals like the repressive signal of high Pi levels and a concomitant high auxin exposure that promotes growth and questioned whether these complex signals might activate known molecular players in root hair polar growth. Under these conditions, RSL2 expression (but not RSL4) is activated linked to ROS production and root hair growth. On the other hand, by blocking ROS production derived from the NADPH Oxidase C (or RBOHC for RESPIRATORY BURST OXIDASE HOMOLOG C) and ROS production from Secreted type-III Peroxidases (PERs), it was possible to repress the auxin growth-promoting effect. This study identifies a new layer of complexity between auxin, Pi nutrient availability and RSL2/RSL4 transcription factors all acting on ROS homeostasis and growth at the root hair level.
Conflicting Auxin-Phosphate Signals Impact on RSL2 Expression and ROS-Homeostasis Linked to Root Hair Growth in Arabidopsis
Here, we examined by which mechanism root hairs integrate conflicting growth-signals like the repressive high Pi-level clue and a concomitant high auxin exposure that should promote growth and questioned if these complex signals might activate known molecular players in polar growth.
ROS Regulation of Polar Growth in Plant Cells
Plant physiology, 2016
Root hair cells and pollen tubes, like fungal hyphae, possess a typical tip or polar cell expansion with growth limited to the apical dome. Cell expansion needs to be carefully regulated to produce a correct shape and size. Polar cell growth is sustained by oscillatory feedback loops comprising three main components that together play an important role regulating this process. One of the main components are reactive oxygen species (ROS) that, together with calcium ions (Ca(2+)) and pH, sustain polar growth over time. Apoplastic ROS homeostasis controlled by NADPH oxidases as well as by secreted type III peroxidases has a great impact on cell wall properties during cell expansion. Polar growth needs to balance a focused secretion of new materials in an extending but still rigid cell wall in order to contain turgor pressure. In this review, we discuss the gaps in our understanding of how ROS impact on the oscillatory Ca(2+) and pH signatures that, coordinately, allow root hair cells a...
PFT1-controlled ROS balance is critical for multiple stages of root hair development in Arabidopsis
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RBOH-mediated ROS production facilitates lateral root emergence in Arabidopsis
Development (Cambridge, England), 2016
Lateral root (LR) emergence represents a highly coordinated process in which the plant hormone auxin plays a central role. Reactive oxygen species (ROS) have been proposed to function as important signals during auxin-regulated LR formation, however their mode of action is poorly understood. Here, we report that Arabidopsis roots exposed to ROS show increased LR numbers due to the activation of LR pre-branch sites and LR primordia (LRP). Strikingly, ROS treatment can also restore LR formation in pCASP1:shy2-2 and aux1 lax3 mutant lines in which auxin-mediated cell wall accommodation and remodeling in cells overlying the sites of LR formation is disrupted. Specifically, ROS are deposited in the apoplast of these cells during LR emergence, following a spatio-temporal pattern that overlaps the combined expression domains of extracellular ROS donors of the RESPIRATORY BURST OXIDASE HOMOLOGS (RBOH) We also show that disrupting (or enhancing) expression of RBOH in LRP and/or overlying roo...
Redox regulation at the site of primary growth: auxin, cytokinin and ROS crosstalk
Plant, Cell & Environment, 2017
To maintain the activity of meristems is an absolute requirement for plant growth and development, and the role of the plant hormones auxin and cytokinin in apical meristem function is well established. Only little attention has been given, however, to the function of the reactive oxygen species (ROS) gradient along meristematic tissues and its interplay with hormonal regulatory networks. The interdependency between auxin-, cytokinin-, and ROS-related circuits controls primary growth and development while modulating plant morphology in response to detrimental environmental factors. Because ROS interaction with redox-active compounds significantly affects the cellular redox gradient, the latter constitutes an interface for crosstalk between hormone and ROS signalling pathways. This review focuses on the mechanisms underlying ROSdependent interactions with redox and hormonal components in shoot and root apical meristems which are crucial for meristems maintenance when plants are exposed to environmental hardships. We also emphasize the importance of cell type and the subcellular compartmentalization of ROS and redox networks to obtain a holistic understanding of how apical meristems adapt to stress.
Apoplastic Reactive Oxygen Species Transiently Decrease Auxin Signaling and Cause Stress-Induced Morphogenic Response in Arabidopsis
PLANT PHYSIOLOGY, 2011
Reactive oxygen species (ROS) are ubiquitous signaling molecules in plant stress and development. To gain further insight into the plant transcriptional response to apoplastic ROS, the phytotoxic atmospheric pollutant ozone was used as a model ROS inducer in Arabidopsis (Arabidopsis thaliana) and gene expression was analyzed with microarrays. In contrast to the increase in signaling via the stress hormones salicylic acid, abscisic acid, jasmonic acid (JA), and ethylene, ROS treatment caused auxin signaling to be transiently suppressed, which was confirmed with a DR5-uidA auxin reporter construct. Transcriptomic data revealed that various aspects of auxin homeostasis and signaling were modified by apoplastic ROS. Furthermore, a detailed analysis of auxin signaling showed that transcripts of several auxin receptors and Auxin/Indole-3-Acetic Acid (Aux/IAA) transcriptional repressors were reduced in response to apoplastic ROS. The ROS-derived changes in the expression of auxin signaling genes partially overlapped with abiotic stress, pathogen responses, and salicylic acid signaling. Several mechanisms known to suppress auxin signaling during biotic stress were excluded, indicating that ROS regulated auxin responses via a novel mechanism. Using mutants defective in various auxin (axr1, nit1, aux1, tir1 afb2, iaa28-1, iaa28-2) and JA (axr1, coi1-16) responses, ROS-induced cell death was found to be regulated by JA but not by auxin. Chronic ROS treatment resulted in altered leaf morphology, a stress response known as "stress-induced morphogenic response." Altered leaf shape of tir1 afb2 suggests that auxin was a negative regulator of stress-induced morphogenic response in the rosette.
PFT1, a transcriptional Mediator complex subunit, controls root hair differentiation through reactive oxygen species (ROS) distribution in Arabidopsis
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Root hair morphogenesis is driven by an amalgam of interacting processes controlled by complex signaling events. Redox processes and transcriptional control are critical for root hair development. However, the molecular mechanisms that integrate redox state and transcription are largely unknown.
Oxidative stress tolerance in plants: Novel interplay between auxin and reactive oxygen species signaling
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Mini-Review Mini-Review Auxin and ROS The plant growth regulator auxin has been well known for regulating many growth and developmental processes such as meristem development, cell division, cell elongation and maintenance of polarity. 1,2 More recently, auxin's function has also been connected to plant defense against stress. Oxidative stress is a component of many abiotic stress conditions such as drought, 3 high temperature stress, 4 salinity 5 and heavy metal stress 6 and biotic stress conditions such as herbivory 7 and plant pathogen interactions. 8 During these stress conditions, levels of reactive oxygen species (ROS) increase, potentially resulting in oxidations of DNA, proteins and lipids. During plant adaptation, however, cellular repair machineries reduce at least some of these oxidized macromolecules. At the same time, ROS have additional signaling roles in plant adaptation to the stress (Fig. 1). Auxin and ROS are rapidly altered by environmental stress factors. ROS can have effects on auxin biosynthesis, transport, metabolism and signaling. 9 Major ROS molecules in cells include superoxide anion (O 2 −), hydroxyl radical (•OH), singlet oxygen (1 O 2) and hydrogen peroxide (H 2 O 2). They are produced in
Flavonols regulate root hair development by modulating accumulation of reactive oxygen species in the root epidermis
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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 of one ROS, H2O2, in driving root hair initiation and demonstrated that localized synthesis of flavonol antioxidants control the level of H202 and root hair formation. Root hairs form from trichoblast cells that express RBOHC and have elevated H2O2, compared to 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 than 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 transpo...
Complementary interactions between oxidative stress and auxins control plant growth responses at plant, organ, and cellular level
Journal of Experimental Botany, 2005
Plant stress responses are a key factor in steering the development of cells, tissues, and organs. However, the stress-induced signal transduction cascades that control localized growth and cell size/differentiation are not well understood. It is reported here that oxidative stress, exerted by paraquat or alloxan, induced localized cell proliferation in intact seedlings, in isolated root segments, and at the single cell level. Analysis of the stress-induced mitotic activity revealed that oxidative stress enhances auxin-dependent growth cycle reactivation. Based on the similarities between responses at plant, tissue, or single cell level, it is hypothesized that a common mechanism of reactive oxygen species enhanced auxin-responsiveness underlies the stressinduced re-orientation of growth, and that stressinduced effects on the protoplast growth cycle are directly relevant in terms of understanding whole plant behaviour.
CBL1‐CIPK26‐mediated phosphorylation enhances activity of the NADPH oxidase RBOHC, but is dispensable for root hair growth
FEBS Letters, 2018
Root hairs (RH) are tip growing polarized cells aiding the uptake of nutrients and water into plants. RH differentiation involves the interplay of various hormones and second messengers. Tightly regulated production of reactive oxygen species by the NADPH oxidase RBOHC crucially functions in RH differentiation and Ca 2+-dependent phosphorylation has been implemented in these processes. However, the kinases regulating RBOHC remained enigmatic. Here we identify CBL1-CIPK26 Ca 2+ sensor-kinase complexes as modulators of RBOHC activity. Combined genetic, cell biological and biochemical analyses reveal synergistic function of CIPK26-mediated phosphorylation and Ca 2+ binding for RBOHC activation. Complementation of rbohC mutant RH phenotypes by a S318/322 phosphorylation deficient RBOHC version suggests flexible and alternating phosphorylation patterns as mechanism fine-tuning ROS production in RH development.
The Auxin-Regulated CrRLK1L Kinase ERULUS Controls Cell Wall Composition during Root Hair Tip Growth
Current biology : CB, 2018
Root hairs facilitate a plant's ability to acquire soil anchorage and nutrients. Root hair growth is regulated by the plant hormone auxin and dependent on localized synthesis, secretion, and modification of the root hair tip cell wall. However, the exact cell wall regulators in root hairs controlled by auxin have yet to be determined. In this study, we describe the characterization of ERULUS (ERU), an auxin-induced Arabidopsis receptor-like kinase, whose expression is directly regulated by ARF7 and ARF19 transcription factors. ERU belongs to the Catharanthus roseus RECEPTOR-LIKE KINASE 1-LIKE (CrRLK1L) subfamily of putative cell wall sensor proteins. Imaging of a fluorescent fusion protein revealed that ERU is localized to the apical root hair plasma membrane. ERU regulates cell wall composition in root hairs and modulates pectin dynamics through negative control of pectin methylesterase (PME) activity. Mutant eru (-/-) root hairs accumulate de-esterified homogalacturonan and ex...
Ethylene signaling increases reactive oxygen species accumulation to drive root hair initiation in Arabidopsis
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ABSTRACTRoot hair initiation is a highly regulated aspect of root development. The plant hormone, ethylene, and its precursor, 1-amino-cyclopropane-1-carboxylic acid (ACC), induce formation and elongation of root hairs. Using confocal microscopy paired with redox biosensors and dyes, we demonstrated that treatments that elevate ethylene levels led to increased hydrogen peroxide accumulation in hair cells prior to root hair formation. In two ethylene-insensitive mutants, etr1-3 and ein3/eil1, there was no increase in root hair number or ROS accumulation. Conversely, etr1-7, a constitutive ethylene signaling receptor mutant, has increased root hair formation and ROS accumulation like ethylene-treated Col-0 seedlings. The caprice and werewolf transcription factor mutants have decreased and elevated ROS levels, which are correlated with levels of root hair initiation. The rhd2-6 mutant, with a defect in the gene encoding a ROS synthesizing Respiratory Burst Oxidase Homolog C (RBOHC) and...
Interaction of OsRopGEF3 Protein With OsRac3 to Regulate Root Hair Elongation and Reactive Oxygen Species Formation in Rice (Oryza sativa)
Frontiers in Plant Science, 2021
Root hairs are tip-growing cells that emerge from the root epidermis and play a role in water and nutrient uptake. One of the key signaling steps for polar cell elongation is the formation of Rho-GTP by accelerating the intrinsic exchange activity of the Rho-ofplant (ROP) or the Rac GTPase protein; this step is activated through the interaction with the plant Rho guanine nucleotide exchange factor (RopGEFs). The molecular players involved in root hair growth in rice are largely unknown. Here, we performed the functional analysis of OsRopGEF3, which is highly expressed in the root hair tissues among the OsRopGEF family genes in rice. To reveal the role of OsRopGEF3, we analyzed the phenotype of loss-of-function mutants of OsRopGEF3, which were generated using the CRISPR-Cas9 system. The mutants had reduced root hair length and increased root hair width. In addition, we confirmed that reactive oxygen species (ROS) were highly reduced in the root hairs of the osropgef3 mutant. The pairwise yeast two-hybrid experiments between OsRopGEF3 and OsROP/Rac proteins in rice revealed that the OsRopGEF3 protein interacts with OsRac3. This interaction and colocalization at the same subcellular organelles were again verified in tobacco leaf cells and rice root protoplasts via bimolecular functional complementation (BiFC) assay. Furthermore, among the three respiratory burst oxidase homolog (OsRBOH) genes that are highly expressed in rice root hair cells, we found that OsRBOH5 can interact with OsRac3. Our results demonstrate an interaction network model wherein OsRopGEF3 converts the GDP of OsRac3 into GTP, and OsRac3-GTP then interacts with the N-terminal of OsRBOH5 to produce ROS, thereby suggesting OsRopGEF3 as a key regulating factor in rice root hair growth.
RSL Class Ⅱ Transcription Factors Guide the Nuclear Localization of RHL1 to Regulate Root Hair Development
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Root hairs are important for absorption of nutrients and water from the rhizosphere. The Root Hair Defective-Six Like (RSL) Class II family of transcription factors is expressed preferentially in root hairs and has a conserved role in root hair development in land plants. We functionally characterized the seven members of the RSL Class II subfamily in the rice (Oryza sativa) genome. In root hairs, six of these genes were preferentially expressed and four were strongly expressed. Phenotypic analysis of each mutant revealed that Os07g39940 plays a major role in root hair formation, based on observations of a short root hair phenotype in those mutants. Overexpression (OX) for each of four family members in rice resulted in an increase in the density and length of root hairs. These four members contain a transcription activation domain and are targeted to the nucleus. They interact with rice Root Hairless1 (OsRHL1), a key regulator of root hair development. When heterologously expressed in epidermal cells of Nicotiana benthamiana leaves, OsRHL1 was predominantly localized to the cytoplasm. When coexpressed with each of the four RSL Class II members, however, OsRLH1 was translocated to the nucleus. Transcriptome analysis using Os07g39940-OX plants revealed that 86 genes, including Class III peroxidases, were highly up-regulated. Furthermore, reactive oxygen species levels in the root hairs were increased in Os07g39940-OX plants but were drastically reduced in the os07g39940 and rhl1 mutants. Our results demonstrate that RSL Class II members function as essential regulators of root hair development in rice. Because root hairs make direct contact with the soil, they perform a vital role in the uptake of nutrients and water from the rhizosphere (Dazzo et al., 1984; Gilroy and Jones, 2000). The presence of those hairs greatly
Apoplastic class III peroxidases PRX62 and PRX69 regulate ROS-homeostasis and cell wall associated extensins linked to root hair growth at low-temperature in Arabidopsis thaliana
2021
ABSTRACTRoot Hairs (RHs) growth is highly influenced by endogenous as well as by external environmental signals that coordinately regulate its final cell size. RHs actively expand the root surface responsible for nutrient uptake and water absorption. We have recently determined that RH growth was unexpectedly boosted when Arabidopsis thaliana seedlings are cultivated at low temperatures. It was proposed that RH growth plasticity in response to low temperature was linked to a reduced nutrient availability in the media. Here, we explored the molecular basis of this strong RH growth response by using the Genome Wide Association Studies (GWAS) approach on Arabidopsis thaliana natural accessions. We identified the poorly characterized PEROXIDASE 62 (PRX62) as a key protein triggering this conditional growth under a moderate low-temperature stress. In addition, we identified the related protein PRX69 as an important factor in this developmental process. The prx62 prx69 double mutant and t...
The involvement of reactive oxygen species (ROS) in the cell cycle activation (G 0 -to-G 1 transition) of plant cells
Plant Signaling & Behavior, 2008
Addendum to: Pasternak TP, Ötvös K, Domoki M, Fehér A. Linked activation of cell division and oxidative stress defense in alfalfa leaf protoplast-derived cells is dependent on exogenous auxin.
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