JXB Advance Access originally published online on May 23, 2006
Journal of Experimental Botany 2006 57(8):1829-1834; doi:10.1093/jxb/erj201
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RESEARCH PAPER |
The role of reactive oxygen species in cell growth: lessons from root hairs
1Ecole Pratique des Hautes Etudes, 46 rue de Lille, F-75007 Paris, France
2Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Colney, Norwich NR4 7UH, UK
*To whom correspondence should be addressed. E-mail: rachel.carol{at}ephe.sorbonne.fr
Received 3 March 2006; Accepted 23 March 2006
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Abstract |
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Reactive oxygen species (ROS) play a diversity of roles in plants. In recent years, a role for NADPH oxidase-derived ROS during cell growth and development has been discovered in a number of plant model systems. These studies indicate that ROS are required for cell expansion during the morphogenesis of organs such as roots and leaves. Furthermore, there is evidence that ROS are required for root hair growth where they control the activity of calcium channels required for polar growth. The role of ROS in the control of root hair growth is reviewed here and results are highlighted that may provide insight into the mechanism of plant cell growth in general.
Key words: Arabidopsis, cell growth, reactive oxygen species, root hairs, tip growth
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Introduction |
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Plant cells come in many shapes and sizes, and the form of the cell is often related to its function. Root hair cells are a good example of such a relationship between form and function. Root hairs are long thin extensions growing out perpendicularly from trichoblasts, one of the cell types of the root epidermis. The presence of root hairs greatly increases the surface area of the root available for the absorption of ions and water and for interaction with soil particles and bacteria. To understand more about how plant cells acquire their shape, it is necessary to know more about the mechanisms of cell growth. By studying two recessive Arabidopsis thaliana mutants with altered root hair phenotypes, we have recently shown genetically that both the production and localization of reactive oxygen species (ROS) are part of the growth mechanism that determines the shape of these specialized plant cells.
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Root hairs grow by tip growth |
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Arabidopsis trichoblasts, the hair-forming epidermal cells, produce a small dome or bulge on the outside of the root once they have stopped elongating in the direction of the root axis (Dolan et al., 1994). In Arabidopsis, the site selected to initiate a hair is at the end of the trichoblast nearest the root apex. The hair starts to grow out and away from the root surface by tip growth, i.e. the length of the hair increases while the diameter (
20 µm) remains constant. The narrow hair may grow up to 1000 µm before growth ceases. During tip growth, the cytoplasm of the hair is highly polarized, with secretory vesicles concentrated at the hair tip followed by the organelles required for the production and secretion of new cell wall and plasma membrane materials (Galway et al., 1997; reviewed in Carol and Dolan, 2001). |
An NADPH oxidase is required for root hair tip growth |
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Hairs of the A. thaliana mutant root hair defective 2 (rhd2) are initiated correctly but they do not elongate. The RHD2 gene encodes respiratory burst oxidase homologue C (AtbohC), an NADPH oxidase similar to mammalian gp91phox (Foreman et al., 2003). NADPH oxidases are haem-containing flavoproteins with multiple transmembrane-spanning domains (EC 1.6.3.1 [EC] ; http://pathology.emory.edu/Lambeth/nadphpage.html). The phox91 family is conserved throughout the plant, animal and fungal kingdoms. They have recently been found in red algae including Chondrus crispus (Herve et al., 2006). These enzymes reduce O2 to form the ROS,
, known as superoxide anion. rhd2 roots produce half as much ROS as wild-type roots when measured in a lucigenin-based chemiluminescence assay (Foreman et al., 2003). Visualizing ROS in roots by nitroblue tetrazolium (NBT) staining or 5-(and 6)-chloromethyl-2',7'-dichlorodihydrofluorescein (CM-H2DCF) imaging shows that ROS accumulate at the hair dome and not at the surrounding parts of the wall of the trichoblast upon hair initiation in the wild type (Foreman et al., 2003; Carol et al., 2005). Then as slow tip growth begins, ROS become concentrated at the tip. As the hairs continue to grow, ROS remain focused at the tip, and when the hair stops growing ROS are no longer produced. A similar focusing of ROS at the tips of immature root hairs has been described in maize roots (Liskay et al., 2004). The ROS accumulation characteristic of wild-type hairs is absent or greatly reduced in rhd2 when visualized by the same methods and by spin trapping electron paramagentic resonance (EPR) spectroscopy (Foreman et al., 2003; Renew et al., 2005).
The stunted growth of rhd2 hairs therefore suggests that ROS production by RHD2 is required for hair growth. To prove this further, diphenylene iodonium chloride (DPI) was used. DPI is a compound which covently binds in the reaction centre of flavoproteins such as NADPH oxidases, thus inhibiting their activity (O'Donnell et al., 1993). The growth of wild-type hairs is inhibited by DPI treatment phenocopying rhd2 mutant hairs (Foreman et al., 2003). Equally, ROS acccummulation in wild-type hairs is inhibited by DPI (Carol et al., 2005). This evidence strongly links ROS production to tip growth and shows that an NADPH oxidase producing ROS is a basic requirement for the tip growth of root hairs. The fact that ROS are focused at the tip where growth is occurring also suggests that they may be involved in a shape-forming mechanism as well as growth itself.
An important clue as to the mode of action of ROS in growth was found when trying to complement the Rhd2– phenotype by applying ROS to rhd2 roots, in this case with hydroxyl radicals, OH·. While the exogenous treatment with hydroxyl radicals partially rescued the phenotype by stimulating outgrowth from rhd2 trichoblasts, irregular bulges were formed rather than typical long, thin, wild-type-like hairs (Foreman et al., 2003; P Linstead, L Dolan, unpublished data). This suggested that for a long thin hair to grow, not only is ROS production by RHD2 required, but also the ROS should be produced in the right place.
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SUPERCENTIPEDE1 spatially controls growth via ROS produced by RHD2 |
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The supercentipede1 (scn1) mutant produces multiple hairs from one initiation site (Parker et al., 2000). The root hairs of this mutant are large outgrowths with multiple irregular bulges (Carol et al., 2005). This aspect of the phenotype bears some resemblance to rhd2 treated with OH· or H2O2. scn1 has another defect in that hairs form at ectopic sites on the trichoblast surface. Therefore, SCN1 controls both the position and the shape of hair outgrowths.
The site of ROS production in scn1 root hairs was determined using NBT staining. Unlike wild-type hairs, scn1 hairs do not focus ROS to a single point at the tip of the growing hair. Instead, multiple foci of ROS may appear in a cell and, where several bulges form, ROS are spread diffusely over the whole surface of the outgrowth. The delocalized ROS production is DPI sensitive, indicating that a flavoenzyme is involved. In the context of the double mutant scn1 rhd2, ROS production on the trichoblast surface is absent, strongly suggesting that RHD2 activity is the source of ROS which is delocalized in scn1. The phenotype of scn1 rhd2 also shows that RHD2-produced ROS are responsible for defective growth, as the multiple hair phenotype of scn1 (average number of hairs >3) is suppressed in the mutant, the majority of trichoblasts initiating a single hair (which does not elongate). (Carol et al., 2005).
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A Rho GTPase GDP-dissociation inhibitor spatially regulates hair growth |
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 TopAbstractIntroductionRoot hairs grow by...An NADPH oxidase is...SUPERCENTIPEDE1 spatially... A Rho GTPase GDP-dissociation... Is ROS-mediated cell growth...What are ROS doing...ConclusionReferences |
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SCN1 is a Rho GTPase GDP dissociation inhibitor (RhoGDI) (Carol et al., 2005). These proteins are thought to regulate the GTPase ‘switch’ negatively by maintaining the GTPase in a GDP-bound ‘inactive’ state. Plants have homologues of Rho GTPases called ROPs. There are 11 genes encoding ROP GTPases in Arabidopsis with different expression profiles (reviewed by Vernoud et al., 2003). ROP2 is a positive regulator of Arabidopsis root hair growth: a constitutively active form of ROP2 (and ROP4 and ROP6) increases hair length and isotropic growth, whereas a dominant negative form of ROP2 inhibits hair growth (Jones et al., 2002). ROPs also localize to the growing region of the hair tip (Moledijk et al., 2001; Jones et al., 2002). SCN1/RhoGDI1 is likely to act by regulating a ROP. It can interact with ROP4 and ROP6 in yeast two-hybrid and in vitro assays (Bischoff et al., 2000). One allele of scn1, scn1-2, has a point mutation in the gene which, based on protein homology modelling, is predicted to be in a region of protein–protein interaction. In protein pull-down assays, the same mutation weakens the interaction between RhoGDI and a generic cauliflower Rop (Carol et al., 2005). Furthermore, the scn1-2 mutant root hairs are indistinguishable from two null alleles scn1-1 and scn1-3. These results strongly suggest that SCN1 regulates ROS production via a ROP GTPase. The mislocalization of a ROP2–yellow fluorescent protein (YFP) fusion to a broad region of the plasma membrane in scn1 mutant root hairs and a shift from a plasma membrane to a cytoplasmic localization have been shown (Carol et al., 2005). To summarize, SCN1 controls the growth of hairs by spatially regulating the production of ROS by RHD2 by the intermediate of a ROP.
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Is ROS-mediated cell growth more general? |
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The ROS-mediated growth described here occurs in tip-growing root hairs, but it is possible that this may be a general mechanism for cell growth. First, the roots of rhd2 mutants that lack the RHD2 NADPH oxidase are shorter than wild type, indicating that RHD2 activity is required for diffuse cell growth that occurs during root elongation. Moreover, the components of the mechanism are well conserved families of proteins. The NADPH oxidase with Rho GTPase and GDI work together in the animal neutrophil phagocytic process, and NADPH oxidase and ROPs feature in the plant defence response to pathogen attack (Keller et al., 1998; Torres et al., 1998). Similarities between the phagocytic oxidative burst in animals and the plant defence response have already been pointed out (Lamb and Dixon, 1997; Wojtaszek, 1997). An NADPH oxidase, a ROP, and the Rop regulatory protein Rop GTPase-activating protein 4 are involved in the plant's response to oxidative stress induced by flooding (Baxter-Burrell et al., 2002). However, in ‘normal’ cell growth, in the absence of biological or physical stresses, do ROS have a role?
The tip growth of pollen tubes parallels that of root hairs. As yet, ROS have not been shown to be involved in pollen tube growth. However, speculation that ROS are involved has led to the discovery that pollen grains have intrinsic NADPH oxidase activity. Pollen from 10 weed species, 10 grasses, and 20 trees were tested, and all were found to have intrinsic NADPH oxidase activity (Boldogh et al., 2005). Of the sample tested in a H2DCF-DA fluorescence-based assay, redtop grass Agrostis alba had the highest redox activity and pine (Pinus sp.) the least. In ragweed Ambrosia artemisiifolia, NADPH oxidase was shown to localize to the plasma membrane of the pollen grain by using an antibody that cross-reacts with the mammalian NADPH oxidase involved in the phagocytic oxidative burst. Pollen-borne NADPH oxidase activity was thus shown to be a major cause of inflammation and mucin production in antigen-induced allergic response of lungs. As pollen-derived ROS are produced in lung tissue, it suggests that the pollen protein is immediately activated on finding a favourable environment (Boldogh et al., 2005). While NADPH oxidases may protect pollen grains from environmental stresses, it is probable, although untested, that their presence at the plasma membrane primes the pollen grain for growth once it settles on the stigma of a flower.
The action of Rop GTPases in pollen tube growth has been studied (reviewed by Gu et al., 2002). ROP1 regulates pollen tube growth as dominant negative ROP1, and microinjected anti-ROP1 antibodies inhibit pollen tube growth. Overexpression of ROP1 or expression of constitutively active ROPs cause depolarized pollen tube growth (Kost et al., 1999; Li et al., 1999; Fu et al., 2001). Arabidopsis SCN1/GDI1 reverses the effect of the depolarized growth induced by overexpressing AtROP1 in Nicotiana tabacum tobacco pollen, removing the ROP from its ectopic localization at the plasma membrane (Fu et al., 2001). Given that there are 10 NADPH oxidases in Arabidopsis, 11 ROPs, and three RhoGDIs, it is possible that some combination of these homologues can act together in promoting pollen tube growth as well as root hair growth and stress responses.
Are ROS involved in non-tip growth? rhd2 roots are shorter than wild-type roots, suggesting that ROS are required for the growth of other cell types (Foreman et al., 2003). ROS have been detected in the growing regions of leaves, roots, stems, and germinating embryos by a variety of techniques including histochemical or biochemical techniques (Puntarulo et al., 1988; Schopfer, 1994; Schopfer et al., 2001). The technique of spin trapping EPR was used to show that ROS are present in rapidly growing cells of maize (Zea mays) roots, cucumber (Cucumis sativa), and Arabidopsis seedlings (Liszkay et al., 2004; Renew et al., 2005). By dint of the DPI sensitivity of the ROS production, the action of NADPH oxidase is implicated. In maize primary roots, a plasma membrane NADPH oxidase producing superoxide anions, which are then converted to hydroxyl radicals by the cell wall peroxidase activity, is responsible for the wall loosening effect which leads to a growth rate that can lead to as much as a 50% increase in cell length per hour. The ability to produce ROS is a transient property of root cells passing through the growing zone (Liszkay et al., 2004). The production of ROS as both and H2O2 has been detected in the expansion zone of maize leaf blades. Growth of segments excised from the expansion zones was inhibited by DPI, suggesting that a flavoenzyme such as NADPH oxidase could be involved (Rodriguez et al., 2002). Different redox agents or antioxidants can significantly alter the trichoblast/root hair length ratio, showing that the redox status of cells is important for their final form, with there being some inbuilt plasticity (Sánchez-Fernández et al., 1997). In summary, there is clear evidence for the participation of ROS in controlling rapid cell growth.
If ROS are involved in basic cell growth, then they might be expected to influence or be influenced by phytohormones. Gravitropism is controlled by auxin. ROS are required in the gravitropic response of maize and Arabidopsis roots, with auxin inducing ROS production (Joo et al., 2001) in a mechanism that requires the activation of phosphatidylinositol 3-kinase (Joo et al., 2005). Auxin promotes the production of ROS in the outer epidermis of maize coleoptiles (Schopfer, 2001) and ROS themselves stimulate their elongation. In contrast, when auxin inhibits maize root growth, there is a decrease in ROS production (Liszkay et al., 2004). As they inhibit germination, abscisic acid (ABA) and far-red light inhibit ROS production in the embryos and seed coats of germinating radish Raphanus sativus, while gibberellin relieves this inhibition (Schopfer et al., 2001). Although not strictly a growth response, the NADPH oxidases, AtrhbohD and AtrhbohF, are known to be necessary for ABA signalling for stomatal closure (Kwak et al., 2003). By extrapolation, therefore, it can be hypothesized that ABA might signal via ROS during primary cell growth (reviewed by Laloi et al., 2004). While there are clear indications that ROS and hormones interact, it is not clear whether this is in specific signalling pathways or in the growth mechanism itself.
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What are ROS doing in cell growth? |
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ROS networks of production and action are extremely complex (reviewed by Mittler et al., 2004) so there are many points at which ROS can be regulated or have their effect. Tip-high calcium gradients are a feature of polarized growth in both root hairs and pollen tubes (Pierson et al., 1996; Bibikova et al., 1997; Wymer et al., 1997). Creating an ectopic site of growth can be done by artificially releasing Ca2+ in root hairs (Bibikova et al., 1997), thus altering the shape of growth. In Arabidopsis, ROS stimulate the entry of Ca2+ into the cell in a manner characteristic of a calcium plasma membrane hyperpolarization-activated Ca2+ (HACC) channel (Foreman et al., 2003). In rhd2 hairs, the calcium channel activity is present but a Ca2+ gradient is not built up, suggesting that ROS are required to stimulate Ca2+ influx. NADPH oxidases have an EF-hand, a protein motif which can bind Ca2+ and thus regulate the protein activity. NADPH oxidases extracted from tomato (Solanum lycopersicum) membranes can be regulated in vitro by addition of calcium (Sagi and Fluhr, 2001). ROS may therefore regulate Ca2 influx and, in turn, be regulated by Ca2 in a feedback loop.
ROS alter cell wall properties. Apoplastic ROS induce cell wall extension or creep in vivo and in vitro in maize, cucumber, soybean, sunflower, and Scots pine seedlings (Schopfer et al., 2001), and in maize roots (Lizskay et al., 2004). Hydroxyl radicals react with and cleave long chain polysaccharides that make up the plant cell walls, such as pectin, homogalacturonan, and xyloglucan in vitro (Fry et al., 2001). By profiling the characteristic residues formed after NaB3H4 treatment of cell wall polymers extracted from citrus and tamarind in vitro, it was possible to show that ROS-induced loosening of cell walls is part of the natural ripening process in pear fruit (Fry et al., 2001).
From a genetic point of view, scn1 and rhd2 are known to interact with other root hair mutations (Parker et al., 2000). Therefore, these mutants may give more information on how ROS production and localization affect cell growth. For example, SCN1 interacts synergistically with RHD3, with scn1 rhd3 having a hairless root (rhd3 hairs are curly). RHD3 is a GTP-binding protein likely to be involved in secretion required for cell enlargement, as the rhd3 mutant is dwarf (Wang et al., 1997; Zheng et al., 2004). SCN1 acts synergistically with TIP1 and COW1 depending on the criteria being measured; TIP1 is an S-acyl transferase (Hemsley et al., 2005) and COW1 is a phosphatidylinositol transfer protein (Böhme et al., 2004). This suggests then that lipid modification and/or signalling may be important for SCN1 action in regulating RHD2 production of ROS.
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Conclusion |
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Traditionally ROS production by plants has been associated with responses to physiological stress and defence mechanisms against pathogen attack. Now it is known that ROS have a more ‘benign’ and essential role in a basic mechanism of cell growth and in the moulding of cell shape. This fundamental role in cell growth is likely to be more widespread than the polarized tip growth of root hairs. The combination of techniques such as fluorescence imaging and spin trapping EPR for the in vivo quantification of ROS in non-stressed plants will be important. The further study of existing or new mutants and the characterization of the activities of the producers, the regulators, and the targets of ROS will help to show whether ROS have a much more fundamental role in plant cell growth.
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Acknowledgements |
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This work was supported from a BBSRC grant in aid to the John Innes Centre and a grant from the Genes and Developmental Biology Committee of the BBSRC, UK.
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Abbreviations |
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DPI, diphenylene iodonium chloride; EPR, electron paramagnetic resonance; NBT, nitroblue tetrazolium; RhoGDI, Rho GTPase GDP dissociation inhibitor; ROS, reactive oxygen species.
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V. Meyer, R. A. Damveld, M. Arentshorst, U. Stahl, C. A. M. J. J. van den Hondel, and A. F. J. Ram Survival in the Presence of Antifungals: GENOME-WIDE EXPRESSION PROFILING OF ASPERGILLUS NIGER IN RESPONSE TO SUBLETHAL CONCENTRATIONS OF CASPOFUNGIN AND FENPROPIMORPH J. Biol. Chem., November 9, 2007; 282(45): 32935 - 32948. [Abstract] [Full Text] [PDF]
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