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First published online July 22, 2005; 10.1104/pp.105.060061 Plant Physiology 138:2061-2074 (2005) © 2005 American Society of Plant Biologists A Role for Auxin Redistribution in the Responses of the Root System Architecture to Phosphate Starvation in Arabidopsis1Laboratoire de Biochimie and Physiologie Moléculaire des Plantes, Unité Mixte de Recherche 5004, Institut National de la Recherche Agronomique/Centre National de la Recherche Scientifique/Ecole Nationale Supérieure Agronomique de Montpellier/Université Montpellier 2, F–34060 Montpellier cedex 1, France (P.N., G.C., M.R., P.D.); Laboratoire d'Ecophysiologie des Plantes sous Stress Environnementaux, Unité Mixte de Recherche 759, Institut National de la Recherche Agronomique/Ecole Nationale Supérieure Agronomique de Montpellier, F–34060 Montpellier cedex 1, France (B.M.); and Laboratory of Plant Physiology and Biochemistry, University of Antwerp, Campus Drie Eiken, B-2610 Wilrijk, Belgium (A.A., H.V.O.)
The changes in root system architecture (RSA) triggered by phosphate (P) deprivation were studied in Arabidopsis (Arabidopsis thaliana) plants grown for 14 d on 1 mM or 3 µM P. Two different temporal phases were observed in the response of RSA to low P. First, lateral root (LR) development was promoted between days 7 and 11 after germination, but, after day 11, all root growth parameters were negatively affected, leading to a general reduction of primary root (PR) and LR lengths and of LR density. Low P availability had contrasting effects on various stages of LR development, with a marked inhibition of primordia initiation but a strong stimulation of activation of the initiated primordia. The involvement of auxin signaling in these morphological changes was investigated in wild-type plants treated with indole-3-acetic acid or 2,3,5-triiodobenzoic acid and in axr4-1, aux1-7, and eir1-1 mutants. Most effects of low P on RSA were dramatically modified in the mutants or hormone-treated wild-type plants. This shows that auxin plays a major role in the P starvation-induced changes of root development. From these data, we hypothesize that several aspects of the RSA response to low P are triggered by local modifications of auxin concentration. A model is proposed that postulates that P starvation results in (1) an overaccumulation of auxin in the apex of the PR and in young LRs, (2) an overaccumulation of auxin or a change in sensitivity to auxin in the lateral primordia, and (3) a decrease in auxin concentration in the lateral primordia initiation zone of the PR and in old laterals. Measurements of local changes in auxin concentrations induced by low P, either by direct quantification or by biosensor expression pattern (DR5::  -glucuronidase reporter gene), are in line with these hypotheses. Furthermore, the observation that low P availability mimicked the action of auxin in promoting LR development in the alf3 mutant confirmed that P starvation stimulates primordia emergence through increased accumulation of auxin or change in sensitivity to auxin in the primordia. Both the strong effect of 2,3,5-triiodobenzoic acid and the phenotype of the auxin-transport mutants (aux1, eir1) suggest that low P availability modifies local auxin concentrations within the root system through changes in auxin transport rather than auxin synthesis.
Changes in mineral nutrient availability and heterogeneous distribution in the soil induce in plants various adaptive mechanisms, among which the plasticity of root development is of crucial importance (Drew, 1975  ; Lynch, 1995; Thaler and Pages, 1998; Farley and Fitter, 1999; Hell and Hillebrand, 2001). In several species, root proliferation in nutrient-rich regions leads to an increased ratio of root surface to explored soil volume, which facilitates the uptake of nutrients (Drew, 1975; Robinson, 1994). However, the root system architecture (RSA) does not respond the same way to all nutrients (Drew, 1975; Farley and Fitter, 1999). For instance, nitrate availability does not affect the elongation of the primary root (PR) of Arabidopsis (Arabidopsis thaliana), but determines both emergence and elongation rate of lateral roots (LRs; Zhang and Forde, 1998; Zhang et al., 1999). Iron limitation decreases the growth of LRs but increases their density (Moog et al., 1995), and induces the formation of supernumerary root hairs (Schmidt and Schikora, 2001). Phosphate (P) availability also has a strong effect on RSA, which may significantly differ from that of other ions. In Arabidopsis, P starvation has been shown to affect growth of the PR and the initiation and elongation of LRs (Williamson et al., 2001; Linkohr et al., 2002; López-Bucio et al., 2002, 2005; Al Ghazi et al., 2003), and to stimulate formation of root hairs (Bates and Lynch, 1996). In Phaseolus vulgaris, P deficiency affects the growth angle of basal roots (Bonser et al., 1996), whereas it promotes the formation of proteoid roots in Lupinus albus (Johnson et al., 1994, 1996).
In addition to the apparent complexity of the changes in root development induced by P starvation, the signaling pathways triggering these modifications remain mostly obscure. Although specific regulatory mechanisms related to the sensing of the external P availability or internal P status of the plant have to be envisaged, increasing evidence also suggests that hormones play a key role in mediating the P starvation effects on RSA. Because auxin is strongly involved in root development, a possible role of this hormone in the response of root development to P limitation has been proposed (López-Bucio et al., 2002 To further address this question, we carried out an in-depth analysis of the possible roles of auxin in mediating the RSA response to low P. This included daily analysis of several RSA parameters from day (d) 7 to d 14 after sowing, on both wild-type plants treated or not with auxin or auxin-transport inhibitor, and three different mutants altered in auxin response pathways. This provided a large set of data that allowed us to unravel complex interactions between root architecture parameters, auxin, and P starvation response. We show here the main outcomes of this work, i.e. that many effects of P starvation on RSA (PR shortening, inhibition of LR primordia initiation, stimulation of LR primordia activation, young LR elongation) could be explained by auxin redistribution within the root system (increased accumulation in the PR apex, the initiated lateral primordia, and in young LRs, and decrease in auxin concentration in the lateral primordia initiation zone of the PR and in old laterals). A model summarizing these hypotheses of a significant redistribution of auxin in the RSA response to P limitation is presented.
P Starvation Only Transiently Promotes Arabidopsis LR Growth A temporal analysis of the RSA of wild-type Arabidopsis seedlings grown either on high (1 mM) or low (3 µM) P medium was carried out from d 7 to d 14 after germination. Two different phases were observed (Fig. 1). First, from d 7 to d 10, low P availability did not modify PR growth (Fig. 1, B and E) but clearly promoted LR elongation. P-starved plants produced more LR than control plants (Fig. 1D), and these roots grew faster (Fig. 1F). Thereafter, from d 11 onward, all measured RSA parameters were negatively affected by P starvation, including a fast and significant slowing down of LR appearance and elongation (Fig. 1, D and F), and a more delayed decrease in PR elongation (Fig. 1E). These responses finally led to a significant decrease in total and LR lengths (Fig. 1, A and C). In addition, when measured at d 14, P starvation also induced a significant decrease in diameter of PR and in total leaf area (data not shown).
P Starvation Inhibits the Initiation of Lateral Primordia on the PR But Markedly Stimulates Their Activation
The contrasting effect of P starvation on the total number of visible laterals (increase before d 9 and decrease after d 11 relative to +P) was further investigated using transgenic plants expressing the
Significant changes between P-starved and control plants were also observed concerning second-order lateral primordia, located on primary laterals (Fig. 3). As on the PR, low P availability led at d 14 to a decrease in the total number of initiated primordia in old laterals (i.e. >1.5 cm). However, the opposite was found in younger laterals (i.e. <1 cm). This shows that the consequences of P starvation on lateral primordia initiation are not always associated with an inhibitory effect but also somewhat depend on the status of the root itself.
Auxin Alters the RSA Response to P Starvation, Even at Later Stages When the Overall Plant Growth Is Severely Affected
Results reported above and published data suggest that auxin may be involved in some aspects of root adaptive response to P starvation. To unravel its role, we performed an additional series of experiments, similar to that described in Figure 1, but including various auxin response mutants (axr4, aux1, and eir1) and exogenous indole-3-acetic acid (IAA) or auxin-transport inhibitor (TIBA) applications. The IAA and TIBA concentrations (0.1 µM for both) were selected on the basis of preliminary work performed on plants cultivated on high P medium and treated with a wide range of IAA levels (data not shown). Both hormone-treated wild-type and mutant plants displayed the expected changes in RSA already characterized in previous reports (Fig. 4). For instance, the IAA-treated plants presented a reduced primary root length (Evans et al., 1994
At different time points during the P starvation treatments, several RSA parameters appeared to be strongly affected by the IAA or TIBA treatments as well as by a mutant background. We focused on the RSA data obtained at d 9 and d 14 (Figs. 5 and 6, respectively) because these two time points are illustrative of the two phases of the root response to P starvation identified from the experiment shown in Figure 1. At both time points, d 9 (data not shown) and d 14 (Table I) statistical analyses were conducted. ANOVA indicated that all 17 RSA parameters were highly significantly affected by the hormonal treatments or in the mutants as compared to the wild type at d 14, whereas only 10 of them responded to P starvation (Table I). Interestingly, 12 RSA parameters were strongly affected by the hormonal treatmentxP starvation interaction, showing that auxin and P availability did not act independently.
At d 9, LR growth was stimulated by low P availability, and both LR density and elongation rate were higher in starved plants than in controls (Fig. 5), as observed previously in the independent experiment of Figure 1. However, IAA treatment and all investigated mutations suppressed or moderated the positive effect of P starvation on both parameters of LR growth, at the exception of the axr4 mutation. In this mutant, the increase in LR density by low P was prevented, but not the stimulation of LR elongation rate (Fig. 5). At d 14, the negative effects of P starvation on growth of primary and LR noticed in the experiment of Figure 1 were confirmed (Fig. 6). At the same time, IAA or TIBA treatments and the various mutations strongly modified most of these effects. Exogenous IAA supply amplified the decrease in PR elongation rate induced by low P, while TIBA treatment or all three mutations prevented this decrease (Fig. 6). Concerning LR density, the detrimental effect of P starvation was reverted by IAA or suppressed by TIBA treatments (Fig. 6). The increased LR density in IAA-treated plants was mainly due to a higher number of LR and not to a strongly reduced PR length (although the elongation rate of the PR begins to be drastically reduced at d 14; Fig. 6). Furthermore, TIBA or the axr4, aux1, and eir1 mutations profoundly altered the action of P starvation on the LR elongation rate since they all result in a marked increase of this parameter in P-starved plants compared with unstarved plants (Fig. 6). Some of these observations made at d 14 are particularly striking because they indicate that, depending on the auxin status of the plant, LR growth can still be either unaffected or even stimulated by P starvation. As an example, P starvation strongly stimulated LR elongation rate in the presence of TIBA, with no effect on either LR density or PR elongation rate (Fig. 6). This suggests that the slowing down of root growth after 11 d of culture on low P medium (Fig. 1) was not simply caused by nutrient shortage but represented a true adaptive response in which auxin might play a crucial role. The situation appeared to be different in the shoot, where the decrease in total leaf area resulting from growth on low P medium was unaffected by all treatments or mutations (Fig. 7), suggesting that the effect of P starvation on shoot growth might be independent of auxin signaling.
A more detailed temporal study of the effect of auxin on both responses of PR elongation rate and LR density to low P showed that this hormone did not act in modifying the timing of the phase shifts induced by P limitation but rather in modulating the magnitude of the response to low P (Fig. 8). Indeed, the PR elongation rate in plants grown on low P started to decrease at roughly the same time point regardless of the presence or the absence of IAA in the medium, but the amplitude of this effect was markedly higher in IAA-treated plants (Fig. 8A). Similarly, the fact that IAA reverted the negative effect of low P on LR density at d 14 cannot be explained by a delayed appearance of LR in IAA-treated plants grown on high P (Fig. 8B).
The Free IAA Levels in Different Parts of the Root Are Significantly Modified by P Starvation The results detailed above suggest that auxin plays a central role in the response of RSA to P starvation. At least two hypotheses could be generated from the data obtained at d 14. First, low P availability induces increased transport and accumulation of auxin into the PR apex, which triggers the slowing down of PR growth in P-starved plants. This is supported by the fact that IAA supply amplified the negative effect of P starvation on PR elongation rate, while inhibition of IAA transport (TIBA, aux1, eir1) or reduced sensitivity to auxin (axr4) suppressed it (Fig. 6). Second, P starvation results in a decreased auxin accumulation in the primordia initiation zone of the PR. This would explain why low P availability reduces primordia initiation (Fig. 2, A and B) and LR density at d 14, which is reverted by IAA supply (Fig. 6). To test the hypothesis that P starvation alters RSA through local variations of auxin concentration in various portions of the root system, free IAA was quantified in different parts of seedlings grown for 14 d on high or low P medium (Fig. 9). Specific analysis of the primordia initiation zone could not be performed due to the difficulty to determine its precise location from macroscopic observations. The data obtained confirmed that, in P-starved plants compared to controls, auxin concentration was significantly increased (by 45%) in the PR apex. Increases in free IAA concentration in response to low P availability were also observed in the whole PR and in young LRs, whereas auxin concentration was decreased in old ones (Fig. 9). IAA concentration in the aerial part was not affected. All these changes were partially or totally prevented by TIBA treatment (Fig. 9), clearly demonstrating that variations in the auxin concentration in response to low P are probably due to changes in transport rather than in de novo synthesis.
To visualize auxin distribution and local accumulation at the microscopic level, we used the auxin-responsive reporter DR5::GUS (Ulmasov et al., 1997 ). A strong GUS activity was detected in the PR apex in both starved and control plants (Fig. 10, A–D). Phosphate depletion induced an increase as well as an expansion of GUS expression, leading to strong staining of the columella and the vascular tissue (Fig. 10, B and D). The LR development was followed from primordia initiation to postemergence in plants cultivated on low or high P medium (Fig. 10, E–P). For plants cultivated on high P medium, a weak GUS staining was systematically detected in stage I and II primordia (Fig. 10, E and G), whereas it was only occasionally observed at stages V and VI (Fig. 10, I and K). Later on, a strong GUS expression was observed at the tips of emerged primordia (Fig. 10M) and in young LR (Fig. 10O). In P-starved plants, a much stronger GUS activity was always observed at the different development stages (Fig. 10, F, H, J, and L), especially prior to emergence (Fig. 10L). Similarly, a stronger and wider expression was observed at the tips of emerged primordia (Fig. 10N) and in young laterals, where GUS activity was also located in the vascular tissue (Fig. 10P). These expression patterns of the DR5::GUS reporter gene thus suggest that P starvation results in an auxin overaccumulation or drastically modifies auxin sensitivity in the apex of the PR, in initiated primordia, and in young LR.
P Starvation Mimics the Effect of Auxin on the Root Phenotype of the alf3 Mutant
The hypothesis of an overaccumulation of auxin in initiated primordia in response to P starvation was further investigated using the alf3 mutant. This mutant is strongly altered in LR development, with a root system consisting of a long PR covered with many arrested LR primordia (Celenza et al., 1995
The RSA Response to Low P Involves Both Stimulatory and Inhibitory Effects on Specific Root Growth Parameters and Is Dependent on Auxin Signaling
In many plant species, it has been shown that low P availability in the external medium strongly alters RSA (Drew, 1975
Our results also delineate contrasting effects of P starvation on LR development with a strong inhibition of primordia initiation combined with a marked stimulation of their activation (Fig. 2, B and C). Such dual effects also occurred on old LR (i.e.>1.5 cm), where appearance of second-order LRs was observed after 14 d of culture on low P medium despite reduced primordia density (Fig. 3). Second-order laterals were never observed for plants grown on high P medium (data not shown). If nutritional regulation of LR elongation has been documented (see above), very little is known concerning the effect of nutrients on the primordia initiation. To date, only high carbon-to-nitrogen ratio has been reported to dramatically repress primordia initiation with little or no effect on the PR (Malamy and Ryan, 2001
Taken together, these root adaptive responses suggest that hormones and, more likely, auxin might be involved. To study its action, we used concentrations of IAA and TIBA that were 1 to 3 orders of magnitude lower than those applied in previous studies (López-Bucio et al., 2002
Not all responses to P starvation seem to result from changes in auxin action. For instance, all mutants and hormone-treated wild-type plants showed a similar decrease in leaf area in response to P starvation as untreated wild-type plants (i.e. around 50% reduction at the end of the experiment; Fig. 7). Another well-documented response of the shoot to P starvation is anthocyanin accumulation (Raghothama, 1999
Our data support the idea that many effects of P starvation on RSA (Figs. 1–3
The action of auxin in triggering the inhibition by low P of the elongation of the PR (point 1 of the model) is suggested first by the observation that exogenous auxin supply amplified this effect (Fig. 6) and, second, by the fact that the axr4 mutant with reduced sensitivity to auxin had similar PR elongation rate at both levels of P supply (Figs. 6 and 8A). Our interpretation is that P starvation stimulates auxin accumulation in the PR apex, which resulted in a reduced elongation rate of the root. This is in agreement with the well-known negative action of auxin on PR elongation (Evans et al., 1994 ; Hobbie and Estelle, 1995; Timpte et al., 1995), and is further supported by our data showing that low P indeed resulted in a higher auxin concentration and an increased activity of the auxin-inducible DR5 promoter in the PR apex (Figs. 9 and 10).
The postulated decrease by P starvation of the auxin concentration in the LR initiation zone of the PR (point 2 of the model) could not be confirmed by direct auxin measurements or visualization of DR5 activity, mostly because of the difficulty in precisely locating this zone. However, low P availability strongly decreased the total number of primordia initiated along the primary axis (Fig. 2, B and C), an effect that certainly explains the lower LR number and density found in P-starved plants at d 14 (Figs. 1 and 6). Because cell cycle reactivation in the xylem pericycle, which leads to the initiation of primordia, is a step of LR development critically dependent on auxin (Casimiro et al., 2001
The hypothesis that P starvation promotes LR development through increased auxin accumulation in initiated primordia or newly emerged young LRs (point 3 of the model) is strongly supported by several lines of evidence. First, low P dramatically stimulated activation of initiated primordia (Fig. 2, B and C), a process relying on the auxin-mediated establishment and activity of a new meristem (Celenza et al., 1995 Although our data are consistent with local changes in auxin concentration in response to low P, we cannot exclude that in the portions of the root system that were only investigated using DR5::GUS expression (primordia initiation zone of the PR and initiated primordia), the effect of low P could be associated with a modified sensitivity to auxin and not to external changes in auxin concentration.
In a recent study, López-Bucio et al. (2005)
Because TIBA strongly altered the effects of P starvation on both RSA (Figs. 5 and 6) and local auxin concentrations (Fig. 9), our model also hypothesizes that the morphological responses of the root system to low P are due to modifications of auxin transport. The clearest example of this may be the earlier appearance (at d 7–9) of LRs in P-starved plants compared with controls (Fig. 1; Fig. 5, LR density). This is postulated to result from an increase in auxin concentration occurring in the initiated primordia and young LRs (Fig. 12). Accordingly, both exogenous IAA supply and axr4 mutation suppressed the promoting effect of low P on LR density at d 9 (Fig. 5). Interestingly, earlier appearance of LR at low P availability is also abolished at d 9 in the aux1 mutant, in which the basipetal auxin transport (from cotyledons or young leaves to the roots) is impaired due to decreased phloem unloading (Swarup et al., 2001
The interpretation of the effects of TIBA or of mutations of auxin transporters on the RSA response to low P in 14-d-old plants might be more challenging because, at this later stage, all parts of the seedlings can potentially synthesize IAA de novo (Ljung et al., 2001
Despite this complexity, several aspects of the P starvation-induced RSA response could be explained by changes in auxin transport. For instance, the decrease in auxin concentration in the primordia initiation zone of the PR and its increase in young laterals could result from enhanced auxin flux from the former to the latter. Phosphorus depletion may act in two different ways, either by increasing basipetal and lateral transport to the initiated primordia or more likely by enhancing the auxin sink activity of newly formed primordia according to the "fountain" model proposed by Benkova et al., (2003)
In conclusion, our data support the hypothesis that many processes of the adaptive response of the RSA to P starvation are triggered by auxin redistribution within the root system. Nevertheless, the proposed model does not explain all the root responses to P starvation that were observed in our experiments. For instance, the increase in auxin concentration found in young LR in response to P starvation might account for the higher elongation rate of laterals in 9-d-old plants cultured on low P medium as compared with controls (Fig. 5). However, this hypothesis is challenged by several observations (Figs. 5 and 6). First, exogenous auxin supply did not stimulate LR elongation rate in unstarved plants. Second, LR elongation was markedly increased by low P in the auxin-resistant mutant axr4. Third, LR elongation rate was drastically modified in both auxin-transport mutants. Taken together, these results suggest that auxin signaling is only partially involved in the response of LR elongation to low P. Other signaling pathways, including those involving other phytohormones, have to be considered. Trull et al. (1997)
Plant Material and Growth Conditions
Arabidopsis (Arabidopsis thaliana) ecotype Columbia-0 (Col-0) and the different mutant strains axr4-1 (CS8018; Hobbie and Estelle, 1995 Seeds were surface-sterilized in 4% (w/v) BAYROCHLOR (Bayrol, Mundolsheim, France), 50% (v/v) ethanol during 10 min, and then washed three times with 100% ethanol and three times in sterile water. Sterile seeds were sown on 12- x 12-cm petri dishes (Greiner Bio-one, Frickenhausen, Germany) containing 40 mL of sterile culture medium, sealed with Parafilm. The high P culture medium contained 0.5 mM CaSO4, 2 mM KNO3, 0.5 mM MgCl2, 0.05 mM NaFe-EDTA, 1 mM KH2PO4, 2.5 mM MES, 50 µM H3BO3, 12 µM MnCl2, 1 µM CuCl2, 1 µM ZnCl2, 30 nM NH4Mo, adjusted to pH 5.7 with 1 N KOH and solidified with 0.8% (w/v) Bactoagar (DIFCO, BD Bioscience, Sparks, MD). All chemicals were purchased from Sigma Chemicals (St. Quentin, France). In low P medium, although KH2PO4 was replaced by 1 mM KCl, the P content was estimated at 3 µM due to the slight P content of Bactoagar. After sowing on either high or low P medium, petri dishes were cold treated at 4°C for 24 h in darkness to promote and synchronize germination and, subsequently, were transferred in a near vertical position to a growth chamber under a temperature of 21.5°C and a photoperiod of 16 h of light (150 µmol m–2 s–1) using fluorescent and metallic halogens lamps. At d 7, a subset of 15 seedlings was transplanted into new petri dishes containing fresh medium (either high or low P medium; five seedlings per plate).
Low and high P culture media were supplemented with either 0.1 µM IAA or 0.1 µM TIBA. These compounds were filter-sterilized and added to medium at 60°C. IAA and TIBA were purchased from Sigma Chemicals.
The root systems of plants grown in vertical agar plates were scanned daily at 300 dpi (EPSON perfection 2450 Photo; Seiko Epson, Nagano, Japan). Root growth parameters were determined after analysis of scanned images using the Optimas image analysis software (MediaCybernetics, Silver Spring, MD) as described by Freixes et al. (2002)
Histochemical analysis of the GUS reporter enzyme activity was adapted from Craig (1992)
The frozen samples were ground in liquid nitrogen and extracted overnight at –20°C in 80% (v/v) methanol. For recovery calculations, 138 pmol of 13C6-IAA (Cambridge Isotope Laboratories, Andover, MA) was added to the samples. After centrifugation (20,000g, 15 min, 4°C), the supernatant was collected and passed through a C18 cartridge (Varian, Harbor City, CA). Afterward, IAA was purified by means of a DEAE-Sephadex A25 cartridge (formic acid conditions; Amersham Pharmacia, Uppsala) coupled to a C18 cartridge. Prior to analyses, samples were methylated by methyl ester (Prinsen et al., 2000
We thank Drs. Catherine Bellini, Paola Grisafi, and Tom Beeckman for kindly providing us seeds of DR5::GUS, alf3, and CycBl::GUS, respectively. We gratefully acknowledge Alain Gojon for stimulating discussion and critical reading of our manuscript. Hugues Baudot and Gaëlle Viennois are thanked for their valuable technical assistance. Received January 24, 2005; returned for revision April 13, 2005; accepted May 10, 2005.
1 This work was supported in part by the Ecogene program of the Institut National de la Recherche Agronomique. 
2 Present address: Laboratoire de Protéomique, UR 1199 Institut National de la Recherche Agronomique, 2 place Viala, F–34060 Montpellier cedex 1 France. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.060061. * Corresponding author; e-mail nacry{at}ensam.inra.fr; fax 33–4–67–52–57–37.
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) or high (1 mM; 
) P concentration on vertically oriented agar plates. Average values (±SD) of eight seedlings, calculated daily from d 7 to d 14 after sowing, are given for the length of the entire root system (A), the PR (B), the cumulated length of the LRs (C), the LR number (D), the PR elongation rate (E), and the LR elongation rate (F). Significant differences (t test) are indicated by asterisks: *, P < 0.05; **, P < 0.01; ***, P < 0.001.
