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. 2006 Jan-Feb;1(1):28–33. doi: 10.4161/psb.1.1.2398

Nitric Oxide Functions as a Positive Regulator of Root Hair Development

María Cristina Lombardo 1,‡, Magdalena Graziano 1,‡, Joseph C Polacco 1,†, Lorenzo Lamattina 1,✉
PMCID: PMC2633697  PMID: 19521473

Abstract

The root epidermis is composed of two cell types: trichoblasts (or hair cells) and atrichoblasts (or non-hair cells). In lettuce (Lactuca sativa cv. Grand Rapids var. Rapidmor oscura) plants grown hydroponically in water, the root epidermis did not form root hairs. The addition of 10 µM sodium nitroprusside (SNP), a nitric oxide (NO) donor, resulted in almost all rhizodermal cells differentiated into root hairs. Treatment with the synthetic auxin 1-naphthyl acetic acid (NAA) displayed a significant increase of root hair formation (RHF) that was prevented by the specific NO scavenger carboxy-PTIO (cPTIO). In Arabidopsis, two mutants have been shown to be defective in NO production and to display altered phenotypes in which NO is implicated. Arabidopsis nos1 has a mutation in an NO synthase structural gene (NOS1), and the nia1 nia2 double mutant is null for nitrate reductase (NR) activity. We observed that both mutants were affected in their capacity of developing root hairs. Root hair elongation was significantly reduced in nos1 and nia1 nia2 mutants as well as in cPTIO-treated wild type plants. A correlation was found between endogenous NO level in roots detected by the fluorescent probe DAF-FM DA and RHF. In Arabidopsis, as well as in lettuce, cPTIO blocked the NAA-induced root hair elongation. Taken together, these results indicate that: (1) NO is a critical molecule in the process leading to RHF and (2) NO is involved in the auxin-signaling cascade leading to RHF.

Key Words: auxin, nitric oxide, root hair, lettuce, arabidopsis, nos1 mutant, nia1, nia2 mutant

Introduction

In the root systems of higher plants, the epidermis is composed of two cell types: (1) root-hair cells or trichoblasts and (2) non-hair cells or atrichoblasts. Root hairs are specialized cell types that function in root anchoring and for increasing the area of soil exploitable by the plant.1 By greatly increasing the total surface area of the root system, root hairs are believed to play an important role in the absorption of water and nutrients from the soil.2 Root hair formation (RHF) can be analysed in phases: cell fate specification, initiation, tip growth and maturation. The identity of epidermal cells, as trichoblast or atrichoblast when protodermic cells, is defined upon entering the elongation phase. At this time, the fate of root epidermal cells is determined by their position with respect to the underlying cortical cells. Atrichoblasts are located over periclinal (outer tangential) wall whereas trichoblasts are located over the clef of two walls formed by adjacent cortical cells.3,4 Due to its versatility, RHF has become a model system for investigation of patterning and morphogenesis in plants.5,6 RHF is affected by hormones, temperature, pH, calcium, iron and phosphorus availability as well as other environmental factors.7

In recent years, nitric oxide (NO) has been described as a bioactive molecule that functions in numerous physiological processes in plants such as regulation of defense-related gene expression and programmed cell death, stomatal closure, seed germination and root development, among others.8,9 Intracellular signaling responses to NO stimulus involve generation of cGMP, cADPR and elevation of cytosolic calcium. However, in many cases a complex network of as yet undeciphered biochemical and molecular mechanisms governs NO-dependent physiological responses.9

Genetic studies have implicated auxins in the process of RHF.10–12 Since recent studies have placed NO among factors involved in lateral, primary and adventitious root development, processes whose underlying mechanisms are under the control of auxins,13,14 it was of interest to explore whether NO participates in the auxin-induced signalling pathway that triggers RHF. Here we report the stimulatory effect of NO on the development of root hairs. Our results indicate that NO takes part in the auxin responses leading to RHF in lettuce and Arabidopsis. In addition, we also demonstrate that endogenous NO plays a role in RHF in Arabidopsis through the analysis of root hair initiation and elongation in NO-depleted WT plants as well as in NO-deficient nos1 and nia1 nia2 mutants.

Materials and Methods

Plant material and growth conditions.

Lactuca sativa cv. Grand Rapids var. Rapidmor oscura seeds were germinated in petri dishes containing water-imbibed filter papers and maintained at 26°C for three days until the root apex was visible. Seedlings were grown hydroponically in water. Treatments with different concentrations (0.1, 1, 10 or 100 µM) of the NO donor sodium nitroprusside (SNP; Merck, Darmstadt, Germany) were performed for three days. For the experiment in Figure 2, seedlings were grown in water for 2 d and then treated with 10 µM SNP or 10 nM 1-naphthyl acetic acid (NAA; Sigma, St. Louis, MO, USA) and/or 1 mM of the NO scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt (cPTIO; Molecular Probes, Eugene, OR, USA) or 10 µM NO2−/NO3− for three more days in hydroponics.

Figure 2.

Figure 2

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Auxin-induced root hair formation is dependent on NO in lettuce. Germinated seeds of lettuce were grown in water for 2 d and treated as indicated for another 3 d. Root hair density (root hairs per mm2) is expressed as mean ± SE (n = 20 seeds from at least three independent experiments) (A) SNP was used at 10 µM, cPTIO was used at 1 mM, NO2−/NO3− at 10 µM each and NAA at 10 nM. (B) Photomicrographs of epidermal cells from the root hair differentiation zone of seedlings grown in water or SNP. Bar = 10 µm.

Arabidopsis thaliana wild type seeds were obtained from Arabidopsis Biological Resource Center (Ohio State University, Columbus); nos1 and nia1 nia2 mutants were a kind gift from Nigel Crawford (University of California, San Diego). All Arabidopsis genotypes used in this study are in Col-0 background. Seeds were surface sterilized by immersion in 70% (v/v) ethanol for 5 min and 30% (v/v) bleach for 15 min, followed by three rinses in sterile water. Seeds were cold-treated in water at 4°C for 2 d and sown into petri dishes containing ATS medium: 0.7% (w/v) agar, 1% (w/v) Suc, and mineral nutrients according to Wilson et al..15 Petri dishes were incubated in a chamber at 25°C with a photoperiod of 14 h. After four days of growth, seedlings were transferred to fresh medium containing the treatments and were grown for three more days when NO content, root hair number and length were analyzed. Concentrations used were: 0.5 and 1 mM cPTIO and 50 nM NAA. Special attention was paid to analyze RHF only in roots immersed in the medium since RHF is affected by contact with air.

Microscopy.

Roots of lettuce or Arabidopsis were fixed with FAA solution (ethanol:water: formaldehyde:acetic acid, 10:7:2:1, v/v) for 48 h and stained with Toluidine blue. Root hair patterns in lettuce were analysed in cross sections of ten primary root apical segments per treatment. Freehand cross-sections were taken and stained with Toluidine blue. Epidermal cell patterning of the seedling root was analysed on the basis of two areas per root of the root hair zone. Root hair density was estimated by counting root hairs and bulges in the root hair zone of ten roots in the second mm behind the apex. Statistical significance of differences between mean values was determined using Student's t test. Photographs were recorded with a Nikon Coolpix 990 digital camera attached to the microscope. To show the root hair pattern in Arabidopsis roots for each genotype and treatment, dark-field microscopy photographs were taken of ten segments at 5 mm from the root tips.

Detection of endogenous NO.

Arabidopsis seedlings were incubated in 5 µM of the cell-permeable fluorescent probe 3-amino, 4-aminomethyl-2,7-difluorofluorescein diacetate (DAF-FM DA; Calbiochem, San Diego, CA, USA) in 20 mM Hepes-NaOH (pH 7.5) for 30 min. Thereafter, roots were washed three times with fresh buffer and examined by epi-fluorescence (DAF-FM DA excitation 490 nm, emission 525 nm) and bright-field microscopy in an Eclipse E 200 microscope (Nikon, Tokyo).

Results

Nitric oxide induces root hair formation in lettuce.

In lettuce seedlings growing hydroponically in water, very few root hairs were developed. In an attempt to elucidate the role of NO in RHF, we performed a dose-response experiment with the NO donor SNP. The surface of the primary root covered with root hairs was dramatically increased (400%) by treatment with 10 µM SNP (Fig. 1A), while the length of the primary root was unaffected at this concentration of SNP (Fig. 1B). Figure 1C shows that RHF in untreated primary roots (control) is strictly confined to the transition zone between root and hypocotyl. However, treatment with 10 µM SNP resulted in almost the entire root surface being covered by root hairs (Fig. 1C).

Figure 1.

Figure 1

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Nitric oxide induces root hair development in lettuce (Lactuca sativa L.). Lettuce seeds were germinated in water and when the radicle was 1 mm length, they were transferred to pots and grown hydroponically in water or in the presence of different concentrations of the NO donor sodium nitroprusside (SNP) for 3 d. Root hair density (A) and the length of the primary root (B) were analysed. The means and SE were from three independent experiments (n = 12). Asterisks mean significant difference (p < 0.05). (C) Photographs of representative seedling roots. Bar = 1 mm.

Nitric oxide is involved in auxin-induced root hair formation in Lettuce.

As stated, genetic studies have confirmed auxin-dependence in the process of root hair development.10,12 Taking into consideration that NO is among downstream components in the auxin signalling cascade leading to root development,13,14 we tested the NO requirement for the auxin-mediated RHF. Figure 2A shows that the density of root hairs was significantly increased both by NO and the synthetic auxin NAA. More interestingly, the NO scavenger cPTIO was able to prevent both the NO- and the NAA-mediated induction of RHF, indicating that NO is required for the observed root hair phenotype. Control experiments also confirmed that the NO decomposition products NO2−/NO3− were ineffective in promoting RHF (Fig. 2A). No significant differences were found in primary root growth by any of these treatments (not shown).

Figure 2B (control) depicts a detailed picture of a root epidermis from a 5 d-water-grown seedling. It can be seen that primary root displays almost no RHF in the root hair zone when growing in water (control), whereas bulge formation and expansion of root hair tips becomes evident when 2 d-old seedlings were exposed to 10 µM SNP for three further days (Fig. 2B, SNP). In fact, NO induced a phenotype with nearly all rhizodermal cells differentiated into root hairs. This experiment shows that epidermal cells are competent to form root hairs and to respond to NO stimulus when growing in water. At this stage, NO treatment seems to be sufficient to trigger the differentiation of atrichoblasts to trichoblasts.

The position of root hairs induced by NO was also analysed. For this experiment, lettuce seedlings were grown on filter papers imbibed with in water (control condition) or in 10 µM SNP for four days. Cross sections of primary roots from control treatment showed that only the epidermal cells that lie over the clefs of underlying cortical cells (H position) form root hairs (Fig. 3, control). In contrast, NO exposure caused ectopic RHF as well as a 100% increase in the frequency of RHF in the H position of the primary root (Fig. 3, SNP).

Figure 3.

Figure 3

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NO induces ectopic root hair formation in lettuce. Germinated seeds of lettuce were grown in Petri dishes on filter papers embedded in water (control) or 10 µM SNP for 4 d. Cross sections of control and NO-treated root exhibiting root hair development from trichoblasts (arrows) and atrichoblasts (asterisks) are shown. Photographs are representative of three independent experiments. Bar = 10 µm.

Nitric oxide is involved in root hair development in Arabidopsis.

The results described above indicate that NO is a key molecule in the events leading to RHF in lettuce, and also that NO is involved in the auxin signaling cascade that mediates this process. We next evaluated NO effects on RHF in Arabidopsis in which root hairs are formed in a predictable, position-dependent pattern,4,16,17 and in which characterized mutants deficient in NO synthesis are available. Two Arabidopsis mutants have been shown to be defective in NO production and to display phenotypes in which NO deficiency is implicated. Arabidopsis nos1 has a mutation in a structural gene (NOS1) encoding an NO synthase,18 the enzyme that catalyses the formation of NO from arginine in the presence of O2. It was reported that nos1 generates 20% of the NO produced by the WT progenitor Col-0.18 Arabidopsis double mutant nia1 nia2 is null for nitrate reductase (NR) activity.19 In addition to its reductase activity on nitrate to form nitrite, NR is also able to catalyse the reduction of nitrite to NO.20,21 Thus, we exploited these mutants to determine a role for endogenous NO on RHF in parallel with the analysis of NO depletion in WT plants treated with the NO scavenger cPTIO. In cPTIO-treated WT plants, root hair length was strongly reduced in a dose-dependent manner (Fig. 4A and B). Indeed, microscopic analysis showed that root hair bulges were present but they did not elongate in the presence of cPTIO. Interestingly, root hair elongation was similarly reduced in both NO-production defective mutants (Fig. 4A and B). However, in contrast to our observations in lettuce, neither NO depletion nor SNP treatment in Arabidopsis plants had a significant effect on root hair number (data not shown).

Figure 4.

Figure 4

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Role of endogenous NO on root hair development in Arabidopsis. Arabidopsis seeds were germinated in Petri dishes with ATS medium (nutrient solution with 1% sucrose and 0.7% agar) for 3 d and then transferred to new medium with the treatments for four further days. (A) Representative pictures of roots from untreated WT plants (control), WT plants treated with 0.5 or 1 mM of the NO scavenger cPTIO, and the NO-synthesis deficient mutants nos1 and nia1 nia2. Bar = 0.5 mm. (B) Quantification of root hair length; mean ± SE (n = 20 seeds from at least three independent experiments). (C) NO-specific fluorescence detected with the probe DAF-FM DA in roots from WT and mutants, bar = 1 mm. (D) Photographs showing the localization of DAF-FM DA fluorescence in WT root cells. Note that the fluorescence is located primarily in root hairs and root-hair cell files. Bar = 200 µm.

Endogenous NO in roots of WT, nos1 and nia1 nia2 plants was analysed with the permeable NO-sensitive fluorophore DAF-FM DA. Figure 4C shows that roots from nos1 and nia1 nia2 as well as roots from cPTIO-treated WT plants displayed less NO-dependent fluorescence than control WT roots. Fluorescence was distributed along the root in untreated WT plants, while in NO-depleted WT plants and in the mutants fluorescence was mainly localized to the root tips (Fig. 4C). Interestingly, NO was not homogenously distributed in roots; indeed, it was primarily located in the root-hair cell files and, with stronger intensity, in the root hairs at any stage of development (Fig. 4D).

It is noteworthy that several auxin response mutants of Arabidopsis display a similar phenotype to that generated by NO depletion in which root hair elongation is the main process affected during RHF.10 To assess whether NO is involved in the auxin signalling cascade that leads to RHF in Arabidopsis, we analyzed root hair length and number in NO-depleted WT plants induced by auxins. As previously reported,10 auxin treatment did not produce a significant increase in root hair number (data not shown). However, root hair length was slightly, but significantly induced by 50 nM NAA (Fig. 5A and B). Interestingly, the NO scavenger cPTIO abolished the effect of NAA and inhibited NAA-promoted root hair elongation in a dose-dependent manner (Fig. 5A and B). NAA-treated roots display more NO-dependent fluorescence in roots compared to untreated plants. In addition, cPTIO in combination with the NAA treatment diminished fluorescence to control levels (Fig. 5C). Altogether, these results suggest that NO is an important molecule acting downstream of auxins in the root hair elongation process in Arabidopsis.

Figure 5.

Figure 5

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NO mediates auxin-induced root hair elongation in Arabidopsis. Plants were grown as was specified in the legend of Figure 4. (A) Representative pictures of roots from untreated WT plants (control) and WT plants treated with 50 nM NAA with or without 0.5 or 1 mM of the NO scavenger cPTIO. Bar = 0.5 mm. (B) Quantification of root hair length; mean ± SE (n = 20 seeds from at least three independent experiments). (C) NO-specific fluorescence detected with the probe DAF-FM DA in roots from control, NAA- and NAA plus cPTIO-treated WT plants. Bar = 1 mm.

Discussion

Here we report NO involvement in RHF both in the initiation and the elongation processes in two unrelated dicotyledonous species. Knowledge acquired from behavior of individual species can help in providing new insights to understand common molecular mechanisms involved in regulation of RHF. Our results favour a model in which NO participates in the regulation of root hair elongation and also in determining ectopic RHF from atrichoblasts.

NO has been shown to affect in a noticeable manner the morphology and developmental pattern of roots. NO is involved in the promotion of lateral and adventitious root initiation, among other developmental processes in roots.13,14,22 Interestingly, these NO-mediated effects in roots are under the control of the phytohormone auxin. Genetic and physiological studies have implicated auxins in root hair development.10 In this work we have shown that NO mediates the effect of auxin on RHF, increasing root hair number and elongation in lettuce and promoting root hair elongation in Arabidopsis. In Arabidopsis, it was previously reported that auxins are mainly involved in the regulation of the elongation and not on the initiation of root hairs.10 Indeed, several auxin response mutants of Arabidopsis display a phenotype similar to that generated by NO depletion in which root hair elongation is the main process affected during RHF.10 In addition, we show that auxin treatment stimulated NO accumulation in Arabidopsis roots. This NO production was mainly located in the root-hair cell files. Interestingly, local NO accumulation during adventitious and lateral root emergence was reported previously.13,14

The results presented in this work support the involvement of NOS-and NR-catalyzed NO synthesis in RHF in Arabidopsis. However, the roles of pH and non-enzymatic NO generation in this system should be also considered. Bethke et al23 demonstrated the existence of apoplastic synthesis of NO from nitrite that requires low pH. Inoue et al.24 demonstrated that low pH induces RHF in young lettuce seedlings. Interestingly, it was clearly demonstrated that low pH (∼4.5) at cell wall bulging of trichoblasts is required at the initiation phase of RHF.5

It has been shown that after initiation of root hairs elongation proceeds by polarized expansion. This expansion involves tip growth and requires biosynthesis of new wall material, localized wall loosening and the flux of vesicles from the endomembrane system to the growing tip. It has been demonstrated that these processes are regulated by the activity of ion channels and by the cytoskeleton.25 The available data indicate that a signaling network operates including reactive oxygen species (ROS), phospholipids and cytoplasmic Ca2+ during root hair initiation and tip growth.26,27 Samaj et al.28 have assembled these components into a model in which ROS produced by NADPH oxidase activates Ca2+ channels at the plasma membrane in the apex of the root tip leading to a tip-focused Ca2+ gradient and subsequent signaling inherent to root hair growth. Interestingly, the requirement of a high cytoplasmic Ca2+ concentration ([Ca2+]Cyt) at the root tip for maintaining its growth rate5 fits with the already established action of NO in modulating Ca2+ level in guard cells: (i) the elevation of [Ca2+]Cyt through the regulation of Ca2+ release from intracellular stores and (ii) the regulation of Ca2+-dependent ion channel activities.29 In another recent report, root hair growth was associated with ROS production through the activation of the MAPK cascade.30 Interestingly, NO has also been shown to be involved in the activation of a MAPK cascade during adventitious root formation.31

Finally, another point that deserves mention is a possible linkage between microtubules and NO during root hair initiation. It is already known that cortical microtubules become randomized during initiation of lateral root primordia in pericycle cells32 as well as during root hair initiation in trichoblasts.32–34 Since NO is involved in lateral root formation14 and in root hair formation and elongation (this work), it is also possible that NO could be mediating the randomization of cortical microtubules which has been shown to precede the dramatic switch in cell polarity during the morphogenetic events described above. In neurons, the involvement of NO in microtubule configuration has already been described.35

Figure 6 describes the potential interactions between NO and other cell signaling pathways that might regulate root hair tip growth. This model is based on that proposed by Samaj et al.28 Here, we summarize different lines of evidence that support NO action on various targets that are proposed as control points of root hair development in the Samaj's model: (i) NO-regulated [Ca2+]cyt and ion channel activity;29,36 (ii) NO-induced activation of MAPK signaling cascade during both plant defense responses against pathogen attack37 and adventitious root formation;31 (iii) NO and ROS participation in the ABA-mediated stomatal closure.38,39

Figure 6.

Figure 6

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Schematic model showing the potential NO target points in the signaling events that lead to root hair tip growth. This simplified model is based on that proposed by Samaj et al.28 Auxin induces NO production through the activation of one or more sources of NO synthesis. The suggested target points for NO action are: (i) Modulation of redox cell state (redox imbalance) as a result of the high affinity between superoxide (O2−) produced by NADPH oxidase and NO, to form peroxyitrite (ONOO−); (ii) activation of guanylate cyclase (GC) and increase of the cGMP level; (iii) activation of Ca2+-channels at the PM and the regulation of [Ca2+]cyt; (iv) signal transduction through the MAPK cascade. All these pathways converge in the remodelling of actin cytoskeleton and activation of vesicle trafficking. Black arrows indicate links established in the induction of root hair development and broken arrows represent already established links in other systems but yet to be demonstrated in root hair tip growth. Abbreviations: cGMP, cyclic GMP; NR, nitrate reductase; NOS, nitric oxide synthase.

There are interesting parallels among the tip growth mechanisms that have been described in specialized cells.40 The growth of pollen tubes toward plant egg cells and the guidance of axons to neural synapses have been shown to share common mechanisms by which external stimuli are sensed and transduced by intracellular signaling pathways that lead to tip growth.40 Prado et al41 reported that NO is involved in the regulation of pollen tube growth and that its effect is mediated via cGMP, as was also reported for the growth of adventitious roots.42 An analogy can be established during nervous system development, where neurons differentiate axons which extend at their tips. NO has been shown to play a fundamental role in neurite outgrowth through a cGMP and MAPK cascade activation.43 Our findings, reported here, demonstrate that NO also plays key functions in the mechanisms underlying root hair development. Therefore, it may be hypothesized that NO is a general factor involved in fast tip-growing cellular systems.

The molecular mechanisms as well as the sensors and second messengers involved in signal transduction cascades that lead to the fine tuning of epidermal cell differentiation are undoubtedly under the control of a complex signalling network. Here we demonstrate that NO functions in RHF in two dicotyledonous species and that NO also plays a central role in RHF associated with hormonal stimulus. Overall, NO appears as a multipurpose signaling messenger that accomplishes its biological functions through its action on multiple targets. Future studies, including those that focus on molecular and physical mechanisms governing interactions among the cytoskeleton, plasma membrane and cell wall, must consider NO as a new and critical player to understand cell differentiation processes in the root epidermis.

Acknowledgements

We thank Dr. Nigel Crawford (University of California, San Diego) for providing us with nos1 and nia1 nia2 seeds. This work was supported by ANPCyT (PICT 1-6496-99 and PICT 1-14457-03 to L.L.); CONICET (grant PIP 898/98 to L.L.); Fundación Antorchas (to L.L. and M.G.) and Institutional grants from UNMdP, Argentina. LL is a fellow from the John Simon Guggenheim Memorial Foundation and J.C.P. is a fellow from the Fulbright Foundation.

Abbreviations

Col-0

Arabidopsis ecotype Columbia

cPTIO

2-(4-carboxyphenyl)-4,4,5,5,-tetramethylimidazoline-1-oxyl-3-oxide

DAF-FM DA

3-amino, 4-aminomethyl-2,7-difluorofluorescein diacetate

NAA

1-naphthylacetic acid

NO

nitric oxide

RHF

root hair formation

SNP

sodium nitroprusside

Footnotes

Previously published online as a Plant Signaling & Behavior E-publication: http://www.landesbioscience.com/journals/psb/abstract.php?id=2398

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