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First published online June 20, 2008; 10.1104/pp.108.121459 Plant Physiology 147:1936-1946 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
Arginase-Negative Mutants of Arabidopsis Exhibit Increased Nitric Oxide Signaling in Root Development1,[W],[OA]Biochemistry Department, University of Missouri, Columbia, Missouri 65211 (T.F., C.D.T., A.T.-M., M.E.H., J.C.P.); Department of Biology, University of Saskatchewan, Saskatoon, Saskatchewan, Canada S7N 5E2 (C.D.T.); Science Complex, University of Guelph, Guelph, Ontario, Canada N1G 2W1 (P.K.D., R.T.M.); Instituto de Investigaciones Biológicas, Universidad Nacional de Mar del Plata, Mar del Plata 7600, Argentina (N.C.-A., L.L.); Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E9 (D.M.B.); and Department of Biophysics and Center of Biotechnology, Universidad Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil CEP 91.501–970 (J.C.P.)
Mutation of either arginase structural gene (ARGAH1 or ARGAH2 encoding arginine [Arg] amidohydrolase-1 and -2, respectively) resulted in increased formation of lateral and adventitious roots in Arabidopsis (Arabidopsis thaliana) seedlings and increased nitric oxide (NO) accumulation and efflux, detected by the fluorogenic traps 3-amino,4-aminomethyl-2',7'-difluorofluorescein diacetate and diamino-rhodamine-4M, respectively. Upon seedling exposure to the synthetic auxin naphthaleneacetic acid, NO accumulation was differentially enhanced in argah1-1 and argah2-1 compared with the wild type. In all genotypes, much 3-amino,4-aminomethyl-2',7'-difluorofluorescein diacetate fluorescence originated from mitochondria. The arginases are both localized to the mitochondrial matrix and closely related. However, their expression levels and patterns differ: ARGAH1 encoded the minor activity, and ARGAH1-driven β-glucuronidase (GUS) was expressed throughout the seedling; the ARGAH2::GUS expression pattern was more localized. Naphthaleneacetic acid increased seedling lateral root numbers (total lateral roots per primary root) in the mutants to twice the number in the wild type, consistent with increased internal NO leading to enhanced auxin signaling in roots. In agreement, argah1-1 and argah2-1 showed increased expression of the auxin-responsive reporter DR5::GUS in root tips, emerging lateral roots, and hypocotyls. We propose that Arg, or an Arg derivative, is a potential NO source and that reduced arginase activity in the mutants results in greater conversion of Arg to NO, thereby potentiating auxin action in roots. This model is supported by supplemental Arg induction of adventitious roots and increased NO accumulation in argah1-1 and argah2-1 versus the wild type.
Nitric oxide (NO) is integral to many plant defense, adaptive, and developmental pathways. In root development, localized increases of NO appear to mediate auxin induction of gravitropic bending in soybean (Glycine max; Hu et al., 2005  ), lateral roots in tomato (Solanum lycopersicum; Correa-Aragunde et al., 2004), root hairs in Arabidopsis (Arabidopsis thaliana; Lombardo et al., 2006), and adventitious roots in cucumber (Cucumis sativus; Pagnussat et al., 2004).
While auxin induces NO accumulation, it is not clear how auxin acts to increase NO or even if this production is enzymatic. For example nonenzymatic production could result from localized auxin-induced increases in acidity (Idam and Newman, 1993
The nia1 nia2 mutant produces less NO, in part, because it lacks NR to reduce nitrate sequentially to nitrite and then to NO. Moreover, nia1 nia2 has drastically lowered nitrite pools for any mitochondrial nitrate-NO conversion. However, Modolo et al. (2006)
Despite the lack of an identified plant NOS gene or gene product, several authors have presented data favoring an Arg-NO link. Corpas et al. (2006)
Arg, as a precursor of spermine, may stimulate NO accumulation indirectly. The polyamine spermine was reported to stimulate NO efflux in Arabidopsis (Tun et al., 2006 We report that T-DNA insertion mutation of either of the two arginase structural genes of Arabidopsis results in increased NO accumulation and the propensity to form lateral and adventitious roots, traits under the control of auxin signaling.
Arabidopsis Produces Two Functional Arginases, Each Targeted to the Mitochondrion Open reading frame (ORF) At4g08870, about 55 kb from the arginase structural gene ARGAH1 (At4g08900; Krumpelman et al., 1995), encodes paralog ARGAH2, based on the criteria of amino acid identity (86%) and functional expression in yeast (Supplemental Fig. S1). No other arginases were identified in the genome. T-DNA disruption mutant argah1-1 (see "Materials and Methods") retained about 85% of total arginase activity induced by 6 d after germination (6 DAG) in the progenitor biovar (Columbia [Col-0], or wild type). argah2-1 seedlings showed a small increase, reaching a plateau at about 4 DAG. Germination, indicated by the arrow (defined as 0 DAG) in Figure 1 , occurred about 2 d after the initiation of imbibition at 22°C. The sum of ARGAH1 and ARGAH2 activities in the mutants was roughly equal to that of the wild type during imbibition, germination, and seedling growth.
While the 311 predicted C-terminal amino acids of ARGAH1 and ARGAH2 exhibit 91% identity, only 13 of the 33 N-terminal amino acids are shared by ARGAH1 and ARGAH2. However, both N termini have predicted mitochondrial transit sequences, according to several programs and annotated in the Arabidopsis SubCellular Proteomic Database (Heazlewood et al., 2005 ). To confirm their predicted mitochondrial location, both proteins were fused at their C termini to the myc epitope tag and expressed transiently (via biolistic bombardment) in tobacco (Nicotiana tabacum) suspension cultured cells. As shown in Figure 2
, immunofluorescence microscopic analysis revealed that both myc-tagged ARGAH1 and ARGAH2 colocalized exclusively with the endogenous E1β-subunit of the pyruvate dehydrogenase complex, a well-known mitochondrial matrix marker protein (Luethy et al., 1995). Neither mock transformation nor omission of anti-myc and/or anti-E1 antibodies yielded immunofluorescence (data not shown). Neither myc-tagged ARGAH1 nor ARGAH2 was immunodetected in transformed tobacco cells permeabilized with digitonin rather than Triton X-100 (data not shown). Therefore, each protein was actually localized in the mitochondrial interior (matrix), since digitonin permeabilizes only the plasma membrane and only cytosolically exposed antigens are accessible to the applied anti-myc IgGs.
Arginase Isoform Expression in Seedlings
Seedling (3 DAG) expression of ARGAH1 and ARGAH2 was examined in transgenic wild-type plants expressing ARGAH1::GUS and ARGAH2::GUS, in which GUS is under the control of the 1.0- and 1.5-kb genome sequence upstream of the initiator ATG of the respective genes (Brownfield et al., 2008
NO Accumulation, Revealed by DAF Fluorescence, Is Enhanced in Seedlings of argah1-1 and argah2-1 For at least two reasons, inactivation of either structural gene could have localized (tissue or organ) effects on Arg metabolism: (1) ARGAH2 encodes the major arginase activity (Fig. 1); (2) ARGAH1, the structural gene for the minor arginase, is active in tissues in which ARGAH2 is not expressed (Fig. 3A). To test a possible relationship between Arg breakdown by arginase and NO production from Arg (or Arg derivative), NO accumulation was examined by DAF fluorescence in whole 3-DAG argah1-1 and argah2-1 seedlings. Seedlings were grown in ATS medium, preloaded for 30 min with the intracellular NO fluorogenic trap DAF, and then exposed for 2 h to 0 or 1 µM naphthaleneacetic acid (NAA). argah1-1 and argah2-1 seedlings consistently showed higher DAF fluorescence than wild-type seedlings, especially upon exposure to 1 µM NAA (Fig. 3B). All three genotypes exhibited some root tip fluorescence. There was clearly high fluorescence in the hypocotyl-root junction of argah1-1. However, total fluorescence was higher in argah2-1 overall, with highest signal in cotyledons, upper hypocotyl, and roots. Intriguingly, there was noticeably reduced fluorescence in the lower hypocotyl, in contrast to argah1-1, which showed highest fluorescence extending from the hypocotyl-root junction into the mid hypocotyl (Fig. 3B). At 5 µM NAA, there was little difference in fluorescence among the wild type, argah1-1, and argah2-1 (data not shown). These patterns of intracellular DAF fluorescence indicate that the arginase mutants accumulate more NO than the wild type (Col-0), especially when exposed to 1 µM NAA for 2 h.
Apoplastic (Bethke et al., 2004 Mitochondrial DAF fluorescence was reported by Guo and Crawford (2005). They observed diminished fluorescence in noa1-1 mitochondria and in wild-type mitochondria treated with the NOS inhibitor L-NAME. In addition, the authors identified a mitochondrial colocalization of NOA1 with MitoTracker. While the data on mitochondrial DAF fluorescence in Figure 3C only reflect the spatial position of the higher DAF signal within the cell, the settings used in each case suggested a higher mitochondrial DAF fluorescence in the arginase disruption mutants than in the wild type (data not shown).
NO was reported to mediate auxin induction of lateral roots in tomato (Correa-Aragunde et al., 2004
Because the arginase mutants had stronger DAF (Fig. 3B) signals than wild-type plants and appeared to have stronger auxin signaling (Fig. 3D), we asked whether auxin-mediated formation of lateral roots was increased in argah1-1 and argah2-1. Seedlings were grown for 3 d on vertical plates and exposed to 0.1 µM NAA for 5 d more. In this experiment, unsupplemented wild-type seedlings produced few lateral roots (length
Model of Potential Metabolic Sources of NO from Arg, an Arg Derivative (Spermine), or Both
We propose the model shown in Figure 5
, in which Arg, or the Arg derivative spermine, or both are sources of NO in Arabidopsis. Tun et al. (2006)
A prediction of this model is that supplementary Arg should have NO-like effects on root development. Wild-type plants were growth arrested at 5 to 10 mM Arg, either as a supplement to ATS or as sole nitrogen source, and Arg growth inhibition and/or lethality were enhanced in the arginase mutants (data not shown). At 3 mM Arg, however, 3-DAG argah1-1 and argah2-1 seedlings exhibited elongated hypocotyls and petioles, curled cotyledons, increased leaf and root thickening, and roots resembling adventitious roots. The wild-type seedling had a much weaker response to Arg: it lacked adventitious roots and root swelling, although there was some lateral root formation and root shortening (Fig. 3F). NO has been reported to mediate auxin induction of adventitious roots in cucumber (Pagnussat et al., 2004 ) and mung bean (Vigna radiata; Huang et al., 2007). Adventitious root formation is under auxin control in Arabidopsis (Sorin et al., 2005). Long petioles and curled cotyledons are also consistent with increased auxin activity in the arginase mutants exposed to Arg. In agreement with increased auxin activity, the root system of Arg-exposed argah1-1 and argah2-1 seedlings exhibited high DAF fluorescence (Fig. 3F). While Arg exposure resulted in more DAF fluorescence in wild-type roots, the response was weaker. These observations are consistent with increased conversion of Arg, or an Arg derivative, to NO in the arginase mutants, leading to a high-auxin phenotype.
As a further test of the model, NO efflux was examined in 3-DAG seedlings with the cell-impermeable fluorogenic NO trap diamino-rhodamine-4M (DAR-4M, herewith designated DAR). The model predicts that argah1-1 and argah2-1 seedlings will exhibit more NO efflux, from higher internal NO stores (Fig. 3B), than wild-type seedlings. The argah1-1 and argah2-1 mutants exhibited approximately twice the DAR signal of the wild type (Fig. 6
). In agreement with the model and the results of Tun et al. (2006)
The arginase mutants argah1-1 and argah2-1 accumulate more NO by three criteria: higher DAF fluorescence (internal signal; Fig. 3B), higher DAR fluorescence (NO efflux; Fig. 6), and enhanced lateral root development (Table I), the latter an NAA response mediated by NO and blocked by the NO scavenger cPTIO (Figs. 3E and 4). Our model (Fig. 5) posits that arginase mutants manifest localized increases in available Arg, which can enter into NO-generating reactions directly, or via polyamines (spermine), or via both precursors. We propose greater intramitochondrial Arg availability, which does not necessarily translate to greater pools on a dry weight basis of whole plants or tissues. Corollaries of the model are at least 2-fold. The first is that arginase mutants are primed or more sensitive to the effects of auxin that are mediated by NO. The second is that their ground state of auxin signaling is higher than in the wild type.
Auxin signaling is enhanced by the criterion of increased expression of DR5::GUS in the arginase mutant backgrounds (Fig. 3D). Also in agreement with the model, supplementary 3 mM Arg had NO-like effects on root development in mutant seedlings, namely, primary root shortening and roots resembling adventitious roots, whereas wild-type seedlings had much weaker responses, no adventitious roots, some lateral root formation, and some root shortening (Fig. 3F). The overall appearance of the arginase-negative seedlings in the presence of 3 mM Arg is strikingly similar to that of the wild type in the presence of the natural auxin precursor indole acetonitrile (Normanly et al., 1997
Another logical test of the model is to examine Arg and polyamine levels. No striking differences were found in whole seedling polyamine content (data not shown). Surprisingly, Arg levels were lower in the mutants (Supplemental Fig. S2). Not shown are other alterations in the amino acid profiles in each mutant. However, without examining cytoplasmic, chloroplastic, and mitochondrial amino acid pools in specific tissues, we can only speculate about how the localized Arg concentrations might be affected. The flux of Arg into various pathways, as opposed to steady-state Arg levels, will have the greatest metabolic impact. We hypothesize that the effective concentration of Arg in the mitochondrion is altered in specific cells of the arginase-negative mutants. A test of this is to use mitochondrial (and other organelle)-specific fluorescent probes for Arg. Arg-induced reporter genes developed in animal cells (Hartenbach et al., 2007
Given that Arg is more available for NO generation in the arginase-negative mutants, is the immediate NO precursor Arg, or Arg-derived polyamine(s)? Supplemental spermine, in addition to Arg, enhanced NO evolution, especially in argah1-1 and argah2-1 (Fig. 6). In no-spermine controls, enhanced NO evolution from the mutants is consistent with increased availability of spermine, derived from Arg in our model. Exogenous and endogenous polyamines, and polyamine conjugates, have a variety of effects on root development (Couée et al., 2004
The model posits a possible NOS-like activity, generating NO directly from Arg. The nox1 NO-overproducing mutant has a complex phenotype, which includes greatly elevated Arg pools (He et al., 2004
NO is produced in response to a large number of stimuli, and the initial NO source in response to those stimuli may vary. Our data indicate that mitochondria, at least in root cells, are significant sources of NO (Fig. 3C). Plastids of Arabidopsis cell culture were reported to exhibit an NO burst in response to iron treatment (Arnaud et al., 2006
The ARGAH1 and ARGAH2 genes are functional by the criteria of arginase promoter-driven GUS expression (Fig. 3A) and functional expression in yeast (Supplemental Fig. S1). Their ORFs share much amino acid similarity, the encoded proteins are targeted to the mitochondrion (Fig. 2), and argah1-1 and argah2-1 mutants have measurable arginase activity in seedling extracts (Fig. 1). Why then does each mutant show a phenotype if the activities are at least partially redundant? Three factors lead to an arginase-reduced, or altered, phenotype in the single mutants. (1) ARGAH1, the structural gene for the minor arginase, is active in tissues in which ARGAH2 is not expressed (Fig. 3A). Loss of ARGAH1 in these tissues is effectively an arginase-null localized phenotype. (2) ARGAH2 encodes the major arginase activity (Fig. 1). In general, elimination of the major ARGAH2 tends to have the greatest effect on fluorescence from DAF (Fig. 3B) and DAR (Fig. 6), indicators of internal and released NO, respectively, on lateral root formation (Table I), and on Arg-induced auxin-like effects and DAF fluorescence (Fig. 3F). (3) ARGAH1 and ARGAH2 do not have congruent expression patterns in seedlings (Fig. 1). In pollen, the minor ARGAH1 is the predominant species. In older plants, ARGAH2 transcript levels respond much more to methyl jasmonate treatment than ARGAH1 (Brownfield et al., 2008
We are continuing attempts to construct argah1 argah2 double mutant nulls and to optimize the inhibition (Kim et al., 2001
Recently, Kolbert et al. (2008)
Plant Growth All Arabidopsis (Arabidopsis thaliana) plants were in the Col-0 background, the genoptype of the wild type. Unless indicated otherwise, plants were grown sterilely on vertical square (100 x 100 mm) petri dishes. Seeds were surface sterilized in 50% commercial bleach (2.6% sodium hypochlorite final concentration) for 5 min and washed five to six times in sterile distilled water. Seeds were sown on ATS medium (Estelle and Somerville, 1987) with 1% Suc and solidified with 0.8% agar. ATS contains a nitrogen source of 9 mM nitrate. If seeds were not previously vernalized, they were incubated for 2 d at 4°C in the dark. Dishes were then placed in a vertical position and incubated at 25°C under a 16/8-h light/dark cycle. Light was provided by 160-W lamps (Philips F72T12/CW/VHO) at 160 µE m–2 s–1 (1,600 lux).
The first plant arginase, ARGAH1 (At4g08900), was cloned earlier from Arabidopsis by functional complementation in yeast (Krumpelman et al., 1995
T-DNA insertion lines for argah1 (SALK_057987; Alonso et al., 2003
Whole seedlings were ground in a cooled mortar and pestle with 1.0 mL of ice-cold 10 mM Tris-HCl (pH 9.0) containing1 mM MnCl2, and the homogenate was centrifuged at approximately 14,000g for 20 min (4°C) in a 1.5-mL microfuge tube. The supernatant was removed with a drawn out glass Pasteur pipette, avoiding the lipid layer, and assayed for arginase activity essentially as described by King and Gifford (1997)
The predicted coding regions of ARGAH1 and ARGAH2 were amplified by PCR and subcloned into XbaI-digested pRTL2/X-myc (Dyer and Mullen, 2001
Antibody sources were as follows: mouse anti-myc antibodies in hybridoma medium (clone 9E10; Princeton University Monoclonal Antibody Facility); rabbit anti-E1 (Luethy et al., 1995 Epifluorescence images of BY-2 cells were acquired using a Zeiss Axioskop 2 MOT epifluorescence microscope (Carl Zeiss) with a Zeiss 63x Plan Apochromat oil-immersion objective. Image capture was performed using a Retiga 1300 CCD camera (Qimaging) and Northern Eclipse 5.0 software (Empix Imaging). All fluorescence images of cells shown in the figures are representative of more than 50 independent (transient) transformations from at least two independent transformation experiments. Figure compositions were generated using Adobe Photoshop CS (Adobe Systems).
Seeds of each genotype (wild type, argah1-1, and argah2-1) were sown on vertical plates in ATS medium and harvested after 4 d (3 DAG). Seedlings were incubated for 30 min in 15 µM DAF (Invitrogen), given two 10-min washes in loading buffer (5 mM MES, pH 5.7, 0.25 mM KCl, and 1 mM CaCl2), and then incubated for 2 h in 0, 1.0, or 5 µM NAA in loading buffer. Flourescence was determined with a binocular Leica Stereoscope MZFLIII with digital camera (Leica Microsystem). Images were processed with Photoshop 7.0 (Adobe Systems) programs.
Seedlings (3 DAG) of each genotype were harvested from vertical plates and incubated for 30 min in freshly prepared 15 mM DAF. All treatments and washes were in loading buffer (5 mM MES, pH 5.7, 0.25 mM KCl, and 1 mM CaCl2). Following two 10-min washes, seedlings were incubated for 2 h in 0, 0.5, or 1.0 µM NAA and then for 15 min in freshly prepared 1 µM MitoTracker Red (Molecular Probes-Invitrogen) followed by three 10-min washes. Imaging of root fluorescence from DAF-FM triazol (excitation, 488 nm; emission measured with a BP 500–550-nm filter) and from MitoTracker Red (excitation, 543 nm; emission measured with an LP 560-nm filter) was carried out with the Zeiss LSM 510 Meta NLO 2-Photon confocal microscope. Images were processed with the LSM Examiner (Zeiss) and Photoshop 7.0 (Adobe Systems) programs.
To determine factors influencing lateral root formation, seeds were sown on vertical plates and at 3 DAG were transferred aseptically to fresh medium containing various additions and grown for 5 d more. Lateral roots (
The procedure was similar to that of Tun et al. (2006)
Seeds of each genotype (Col-0, argah1-1, and argah2-1) were sown on vertical plates in ATS medium and harvested after 4 d (3 DAG). Seedlings were incubated for 1 h at –20°C in 90% ice-cold acetone. Acetone was decanted, and enough GUS staining buffer (Jefferson et al., 1987
The following materials are available in the online version of this article.
We thank Jan Miernyk for providing anti-E1β-subunit (pyruvate dehydrogenase complex) antibodies and Tom Guilfoyle and Gretchen Hagen for the DR5::GUS line. The excellent guidance and help of the staff of the University of Missouri Molecular Cytology Core, under Dr. G. Esteban Fernandez, is gratefully acknowledged. Received April 17, 2008; accepted June 5, 2008; published June 20, 2008.
1 This work was supported by the U.S. Department of Agriculture Cooperative State Research, Education, and Extension Service (grant nos. 2004–38901–02138 and 2006–38901–02138) and by fellowships from the Fulbright and Guggenheim Foundations to J.C.P. and L.L., respectively. 
2 These authors contributed equally to the article.
3 Present address: Columbia (Missouri) Public Schools, 401 Clinkscales Rd., Columbia, MO 65203. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Joe C. Polacco (polaccoj{at}missouri.edu).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.108.121459 * Corresponding author; e-mail polaccoj{at}missouri.edu.
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2 mm). Shown are averages for a minimum of three independent biological replicates, with four seedlings in each replicate, representing each treatment. Different letters indicate significant differences between treatments (ANOVA test, P < 0.05).
