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First published online August 8, 2008; 10.1104/pp.108.125567 Plant Physiology 148:881-893 (2008) © 2008 American Society of Plant Biologists
The Heme Oxygenase/Carbon Monoxide System Is Involved in the Auxin-Induced Cucumber Adventitious Rooting Process1College of Life Sciences, Cooperative Demonstration Laboratory of Centrifuge Technique, Nanjing Agricultural University, and Beckman Coulter Ltd. Co., Nanjing Agricultural University, Nanjing 210095, China
Indole acetic acid (IAA) is an important regulator of adventitious rooting via the activation of complex signaling cascades. In animals, carbon monoxide (CO), mainly generated by heme oxygenases (HOs), is a significant modulator of inflammatory reactions, affecting cell proliferation and the production of growth factors. In this report, we show that treatment with the auxin transport inhibitor naphthylphthalamic acid prevented auxin-mediated induction of adventitious rooting and also decreased the activity of HO and its by-product CO content. The application of IAA, HO-1 activator/CO donor hematin, or CO aqueous solution was able to alleviate the IAA depletion-induced inhibition of adventitious root formation. Meanwhile, IAA or hematin treatment rapidly activated HO activity or HO-1 protein expression, and CO content was also enhanced. The application of the HO-1-specific inhibitor zinc protoporphyrin IX (ZnPPIX) could inhibit the above IAA and hematin responses. CO aqueous solution treatment was able to ameliorate the ZnPPIX-induced inhibition of adventitious rooting. Molecular evidence further showed that ZnPPIX mimicked the effects of naphthylphthalamic acid on the inhibition of adventitious rooting, the down-regulation of one DnaJ-like gene (CSDNAJ-1), and two calcium-dependent protein kinase genes (CSCDPK1 and CSCDPK5). Application of CO aqueous solution not only dose-dependently blocked IAA depletion-induced inhibition of adventitious rooting but also enhanced endogenous CO content and up-regulated CSDNAJ-1 and CSCDPK1/5 transcripts. Together, we provided pharmacological, physiological, and molecular evidence that auxin rapidly activates HO activity and that the product of HO action, CO, then triggers the signal transduction events that lead to the auxin responses of adventitious root formation in cucumber (Cucumis sativus).
Adventitious root formation involves the development of a meristematic tissue after removal of the primary root system. It is well known that adventitious root formation is a complex process that is affected by multiple endogenous factors, including different phytohormones, and various environmental factors, such as light and wounding. Among phytohormones, auxin is particularly important because it can initiate cell division and primordium formation (Doerner, 2000  ; Berleth and Sachs, 2001; Casimiro et al., 2001).
Normally, auxin can induce various distinct developmental responses through direct effects on membrane or cytoskeletal functions or by regulating the expression of many genes or altering related protein activities. For example, DnaJ-like genes have been identified in organisms ranging from yeast to plants and humans. All DnaJ-like proteins are characterized by a J domain, which mediates interactions with Hsp70 in protein folding and the assembly and disassembly of protein complexes. When alternative in vitro morphogenesis processes were induced by auxins, a preferential accumulation of MsJ1, known as an alfalfa (Medicago sativa) DnaJ-like gene, message occurred during root initiation and formation, illustrating a phase-specific modulation during the cell cycle in G2/M (Frugis et al., 1999
Carbon monoxide (CO) is one of the most important reactive trace gases in the troposphere. Since the 17th century, CO has been known as a poisonous gas, also termed the silent killer. However, in the last few years, evidence has accumulated showing that CO is a significant modulator of inflammatory reactions, influencing underlying processes such as cell proliferation and the production of cytokines and growth factors (Verma et al., 1993
As in the animal kingdom, the presence of CO biosynthesis in plants was first reported by Wilks (1959)
In comparison with animal studies, it is generally agreed that CO at high concentrations inhibits plant growth and development (Wilks, 1959
Moreover, it was well known that the depletion of endogenous auxin appears to be a useful tool to investigate the auxin signal transduction pathway (Reed et al., 1998
Hematin- or Hemin-Induced Adventitious Rooting in a Dose-Dependent Manner
We discovered that exogenous hematin or hemin, two HO-1 activators (also termed CO artificial donor) applied in animal and plant research (Lamar et al., 1996
The IAA Depletion Treatment Not Only Prevents Adventitious Root Formation, But Also Decreases Endogenous HO Activity and CO Content
We further applied an inhibitor of basipetal auxin efflux, naphthylphthalamic acid (NPA; 10 µM, auxin depleted), to determine if inhibiting auxin transport would influence the adventitious rooting process, HO activity, and CO content. As expected, NPA applied to decapitated cucumber explants for 2 d before primary root removal, which was reported to reduce basal IAA concentration and inhibit adventitious rooting (Nordström and Eliasson, 1991
The IAA Depletion-Induced Inhibition of Adventitious Root Formation Is Alleviated by Sodium Nitroprusside, IAA, and Hematin Treatments
As was reported previously (Pagnussat et al., 2003
HO Activity and CO Content Are Increased in Response to IAA, Hematin, and SNP Application The IAA- and NO-like effect of applying the HO-1 activator hematin to auxin-depleted cucumber explants first led us to investigate whether changes in the endogenous levels of HO activity and CO content occurred in response to IAA, hematin, and SNP. In our experiment, auxin-depleted explants were treated with 10 µM IAA, hematin, or SNP, and CO synthesis in cucumber hypocotyls was observed (Fig. 4 ). The IAA or SNP treatment induced rapid production of CO and induction of HO activity. The time course experiments showed that, in comparison with water-treated control samples, a rapidly maximum response was discovered as early as 3 h (IAA) or 12 h (SNP) after treatment, followed by a gradual decrease until 24 h. It was interesting that the course of the changes of CO level seemed to parallel the time course of the HO activities. A weaker increased level of CO content and HO activities around 12 h after treatment in the control sample was also observed.
Hematin-induced HO activity and CO content are different from those with IAA or SNP treatment. Figure 4 shows that HO activity and CO content rapidly increased within 6 h after hematin treatment and continued to increase relatively slowly up to 24 h. In fact, the effects of hematin are approximately in a time-dependent manner during 24 h of treatment. We also noted that the enhancement of CO synthesis and HO activity induced by IAA, SNP, or hematin apparently preceded adventitious root formation.
Our further goal was to confirm that the nature of the hematin- or IAA-induced restoration of the inhibition of adventitious root formation induced by IAA depletion is related to HO activity and CO content. Various compounds have been used to inhibit CO synthesis derived from HO in animals and plants. The potent HO-1 inhibitor zinc protoporphyrin IX (ZnPPIX) was first found to inhibit HO activity in both animals and plants (Lamar et al., 1996
In the absence of added hematin or IAA, ZnPPIX-inhibited HO activity and CO content in auxin-depleted cucumber explants were significantly lower than those of control samples at 3 and 24 h (Fig. 5, B and C). When the above samples were treated simultaneously with hematin or IAA, the IAA- or hematin-induced HO activity and CO content were partially blocked. Interestingly, 100% saturation of CO aqueous solution applied for 24 h severely inhibited HO activity in cucumber explants, while 10% aqueous solution exhibited a weaker effect. This was consistent with our previous result (Han et al., 2008 ), which showed that in comparison with cadmium-treated sample, pretreatment with 50% CO saturation aqueous solution was able to decrease the level of HO-1 transcript or HO activity after further cadmium treatment at 12 h in alfalfa seedling roots.
To assess if HO is associated with the auxin response leading to adventitious rooting, we undertook a detailed study on the auxin-induced expression of this enzyme. Hypocotyls of auxin-depleted cucumber explants were tested for HO accumulation, through enzymatic activity determination and immunoblot analysis, at 6 h after the further application of IAA at 0 to 100 µM. The results in Figure 6A
demonstrate that IAA induced HO activity in a dose-dependent manner. Western-blot analysis for HO-1 showed only a single band with a molecular mass of 30 kD, as determined using molecular mass markers (data not shown), a similar value to that reported for the alfalfa root nodules (Baudouin et al., 2004
Effects of NPA, ZnPPIX, and IAA on Adventitious Rooting, and the Expression Profiles of CSDNAJ-1 and CSCDPK1/5 In our experiments, NPA was shown not only to prevent adventitious root formation but also to decrease endogenous HO activity and CO content (Fig. 2). Thus, we first tested whether NPA and ZnPPIX could affect cucumber adventitious root formation and CSDNAJ-1 and CSCDPK1/5 transcripts. In the following experiment, IAA-nondepleted cucumber explants, after removing the primary root, were incubated in water, NPA (10 µM), or ZnPPIX (200 µM) for 2 d. Figure 7, A and B , shows that both NPA and ZnPPIX pretreatment resulted in a significant reduction of adventitious root formation (P < 0.05), with respect to the effect of water pretreatment for another 5 d. Semiquantitative RT-PCR results (Fig. 7, C and D) illustrated that CSDNAJ-1 and CSCDPK1/5 transcripts were slightly enhanced in water treatment within 48 h, but CSDNAJ-1 and CSCDPK5 were totally blocked since the beginning of NPA or ZnPPIX pretreatment. Meanwhile, CSCDPK1 transcript decreased abruptly at 12 h of pretreatment and kept the steady-state amount during the resting time. These results clearly show that ZnPPIX exhibited a similar effect of NPA on the above parameters.
Based on the results described above, the influence of IAA and ZnPPIX applied alone or in combination on adventitious rooting and the expression of CSDNAJ-1 and CSCDPK1/5 were analyzed. IAA induced the expression of CSDNAJ-1 and CSCDPK1/5 during 48 h of treatment (Fig. 7, C and D). Interestingly, the IAA-induced adventitious rooting and expression of CSDNAJ-1 and CSCDPK1/5 were prevented or delayed when ZnPPIX was added simultaneously (Fig. 7). These findings provided preliminary evidence and suggested that endogenous HO and its releasing products could modulate the expression of these genes, which are also involved in the IAA-induced effects, including adventitious rooting and the up-regulation of CSDNAJ-1 and CSCDPK1/5.
Further results also showed that the effect of CO aqueous solution on the restoration of the IAA depletion-induced inhibition of adventitious root formation was dose dependent (Fig. 8A ), as in hematin-treated samples (Fig. 3A), further strengthening the hypothesis that CO produced by HO is responsible for inducing adventitious rooting. The promotion of adventitious root development was maximal with 10% CO saturated solution (approximately equivalent to 18.7 µM; P < 0.01), which was higher than the concentration of hematin applied (10 µM; Fig. 3A).
We next investigated the molecular mechanism underlying adventitious root formation induced by 10% saturated CO aqueous solution in auxin-depleted cucumber explants. Interestingly, we observed that CO content in cucumber hypocotyls was elevated rapidly during the 6-h period when further treated with 10% CO aqueous solution, in comparison with water-treated samples (Fig. 8B), then declined rapidly (data not shown). Furthermore, to compare the mRNA changes of CSDNAJ-1 and CSCDPK, semiquantitative RT-PCR analysis was used. We discovered that the slightly enhanced expression pattern of CSCDPK1 following water treatment for 6 h was approximately similar to that of CSCDPK5, in comparison with the expression of CSDNAJ-1. After the addition of 10% CO aqueous solution, there were apparent increases in the levels of CSDNAJ-1 and CSCDPK1/5 mRNA in auxin-depleted explants (Fig. 8C), all of which were consistent with the restoration of the IAA depletion-induced inhibition of adventitious root formation (Fig. 8A).
Our recent work (Xuan et al., 2007 ) has shown that treatment with exogenous hematin or IAA can result in the strong induction of HO-1 transcript or CO content in wheat root segments, both of which were reversed by the addition of ZnPPIX, a potent inhibitor of HO-1 in both animals and plants. However, whether induction of HO-mediated CO synthesis by auxin is a general response of all plant cells still remains to be determined. In this report, we further demonstrate a previously uncharacterized signaling role for endogenous CO produced by HO, one of which is responsible for mediating IAA-induced adventitious root formation in auxin-depleted cucumber explants.
Akin to NO in animals, CO was recently found to play various important roles in mediating neuronal transmission (Verma et al., 1993
Our previous report found that exogenous CO aqueous solution or its artificial donor hematin was able to induce adventitious rooting of hypocotyl cuttings (primary root removed) from mung bean seedlings (Xu et al., 2006
Although a role for CO in root development was proposed, the cross talk between auxin and endogenous CO still remains to be examined. In the following experiments, we provided further pharmacological, physiological, and molecular evidence that endogenous CO and its synthesizing enzyme HO is a new system in the auxin signaling pathway leading to adventitious rooting.
Previous results showed that apical IAA production could be disrupted by decapitation of the explants, and basipetal transport of auxins was inhibited by NPA (Pagnussat et al., 2003
In human monocytes, the application of hemin was able to induce HO-1 in a dose- and time-dependent fashion, as measured by semiquantitative RT-PCR and flow cytometry (Lang et al., 2005
In a subsequent experiment, molecular evidence also illustrated that IAA treatment induced higher expression of the CSDNAJ-1 and CSCDPK1/5 genes during a 48-h treatment, and these were consistent with the number of adventitious roots observed after another 5-d treatment (Fig. 7). It was previously reported by Frugis et al. (1999) Further molecular evidence showed that besides the inhibition of adventitious root formation, the potent HO-1 inhibitor ZnPPIX as well as NPA decreased the transcription of CSDNAJ-1 and CSCDPK1/5 in cucumber explants, in comparison with the water treatment. Additionally, ZnPPIX treatment could block the IAA responses of these parameters (Fig. 7). Moreover, the application of CO aqueous solution was able to up-regulate the expression of CSDNAJ-1 and CSCDPK1/5 inhibited by IAA-depleted treatment and dose-dependently led to the recovery of adventitious root formation (Fig. 8). Thus, we deduced that DnaJ-1 and CDPK might receive auxin signal or surrounding stimuli to regulate cell division and differentiation in the plant adventitious rooting process. Probably, CO produced by HO acts in a signaling cascade downstream of auxin to induce CSDNAJ-1 and CSCDPK1/5 gene expression and, consequently, cell division and differentiation are activated. Thus, future analysis of HO/CO involvement in the regulation of DnaJ-like genes, CDPK genes, other auxin-induced genes, cell division, and root primordia formation during the adventitious root formation process will surely contribute to our understanding of the molecular mechanisms that regulate root morphogenesis.
The evidence provided here (Figs. 1–8  ) further confirmed that, at least in our experimental conditions, there exists a serial linkage IAA  HO/CO adventitious rooting. Certainly, cloning of the cucumber HO genes and screening of the corresponding mutants will provide greater insights into the mechanisms that regulate adventitious root development and the role of HOs in this process.
Figure 9
shows a representative scheme integrating the different molecules involved in adventitious root formation in cucumber, which were partially described here. Basipetal transport of auxins induces a CO burst synthesized by HO in the basal region of the cucumber hypocotyls. CO then triggers the signal transduction events that lead to the auxin responses of adventitious root formation. Additionally, this pathway might be mediated by the expression of DnaJ-1 and CDPK genes. Meanwhile, previous results have confirmed that IAA triggers a local and transient generation of NO. This NO production might activate a CDPK-dependent transduction pathway, thus leading to adventitious rooting (Pagnussat et al., 2002
In conclusion, the results presented in this report are significant for both fundamental and applied plant biology. Our results suggest that HO/CO, besides exhibiting the antioxidative machinery recently discovered in the plant kingdom (Noriega et al., 2004 , 2007; Liu et al., 2007; Han et al., 2008), also represent a new signal system with significant impact on auxin-induced adventitious root development. Thus, our results open the possibility of using either CO donor or HO activator to improve plant production. As a matter of fact, substantial CO gas, the most common cause of fatal poisoning in the world, is also emitted from plants into the atmosphere. Conversely, the toxic CO gas in the atmosphere, which is usually released by the combustion of fossil fuels, can influence plants. Therefore, it is likely that plant HO/CO, like those in animals, are part of macromolecular complexes in which CO functions within highly localized environments.
Plant Material and Growth Conditions Cucumber seeds (Cucumis sativus ‘Lufeng’) were kindly supplied by Jiangsu Agricultural Institutes. Selected identical seeds were germinated in petri dishes on filter papers imbibed in distilled water, then transferred to an illuminating incubator and maintained at 25°C ± 1°C for 5 d with a 14-h photoperiod at 200 µmol m–2 s–1 intensity. Cucumber seedlings were used either intact (auxin nondepleted, 0 h) or decapitated by excising the apical bud immediately above the cotyledons and incubated in the presence of 10 µM NPA (auxin depleted) for 48 h, before removing the primary root. Cucumber explants were then maintained under the same conditions of temperature and photoperiod for another 5 d in the presence of different media as indicated.
All chemicals were obtained from Sigma unless stated otherwise. Hematin and hemin were used at concentrations of 0.1, 1.0, 10.0, and 100.0 µM. ZnPPIX, a specific inhibitor of HO-1, was used at 200 µM. SNP was used at 10 µM as NO donor. IAA was also purchased from Sigma. NPA, from Chem Service, was used as the auxin transport inhibitor at 10 µM.
The preparation of CO aqueous solution and the determination of CO content in cucumber hypocotyls by gas chromatography and mass spectrometry were carried out according to the method described in our previous reports (Liu et al., 2007
After primary roots were removed, eight cucumber explants were put into a petri dish containing 8 mL of distilled water, varying concentrations of IAA, hematin, hemin, and CO aqueous solution, 10 µM NPA or SNP, 200 µM ZnPPIX, or combination treatments and kept at 25°C ± 1°C for different periods according to the experiment. The concentrations of the above chemicals used for our experiments were supported by other published results (Pagnussat et al., 2002
HO activity from excised cucumber hypocotyls was analyzed using the method described in our previous reports (Liu et al., 2007
Homogenates obtained for HO activity assays were also analyzed by western blotting. Sixty micrograms of protein from homogenates were subjected to SDS-PAGE using a 12.5% acrylamide resolving gel (Mini Protean II System; Bio-Rad) according to Laemmli (1970)
Total RNA was isolated from 100 mg (fresh weight) of excised cucumber hypocotyls by grinding with mortar and pestle in liquid nitrogen until a fine powder appeared and using Trizol reagent (Invitrogen) according to the manufacturer's instructions. DNA-free total RNA (5 µg) from different treatments was used for first-strand cDNA synthesis in a 20-µL reaction volume containing 2.5 units of avian myeloblastosis virus reverse transcriptase XL (Takara) and 1 µM oligo(dT) primer. PCR was performed using 2 µL of a 2-fold dilution of the cDNA, 10 pmol of each oligonucleotide primer, and 1 unit of Taq polymerase (Takara) in a 25-µL reaction volume. Primers used were as follows: for CSDNAJ-1 (accession no. X67695), forward (5'-AGGGTAAGGGTTCTAAAT-3') and reverse (5'-CGACGAGAGACAAGGTAT-3'), amplifying a 390-bp fragment; for CSCDPK1 (accession no. AJ312239), forward (5'-TGCACTGACAAACCAACT-3') and reverse (5'-ACACTCACAATAACCCCT-3'), amplifying a 284-bp fragment; for CSCDPK5 (accession no. AY027885), forward (5'-CAACTTCCCACCTCCTCCG-3') and reverse (5'-GCTTCCCCATCTTCTTTCA-3'), amplifying an 869-bp fragment; for 18s rRNA (accession no. AF206894), forward (5'-CCTGAGAAACGGCTACCACA-3') and reverse (5'-GATCCCGAAGGCCAACAAAA-3'), amplifying a 456-bp fragment. To standardize the results, the relative abundance of 18s rRNA was determined and used as the internal standard. The cycle numbers of the PCR were adjusted for each gene to obtain visible bands on agarose gels. Aliquots from the PCR were loaded on 1.2% agarose gels with the use of ethidium bromide. Specific amplification products of the expected size were observed, and their identities were confirmed by sequencing.
Where indicated, results are expressed as mean values ± SE of at least three independent experiments (n = 20). Statistical analysis was performed using SPSS 8.0 software. For statistical analysis, t test (P < 0.05 or P < 0.01) or Duncan's multiple test (P < 0.05) was chosen as appropriate. Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers X67695, AJ312239, AY027885, and AF206894.
We thank Dr. Evan Evans from the University of Tasmania, Australia, for his kind help in writing the manuscript. Received June 30, 2008; accepted August 1, 2008; published August 8, 2008.
1 This work was supported by the Program for New Century Excellent Talents in University (grant no. NCET–07–0441 to W.-B.S.), the Natural Science Foundation of Jiangsu Province of China (grant no. BK2007157 to W.-B.S.), the 111 Project (grant no. B07030), the National Fund for Fostering Talents of Basic Science (grant no. J0730647 to J.-Y.Q.), and the Student Research Training Project of Nanjing Agricultural University, China (grant no. 0506B07 to W.X.). 
2 These authors contributed equally to the article. 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: Wen-Biao Shen (wbshenh{at}njau.edu.cn). www.plantphysiol.org/cgi/doi/10.1104/pp.108.125567 * Corresponding author; e-mail wbshenh{at}njau.edu.cn.
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ABSTRACT
RESULTS
(BV), CO, and free iron (Fe2+) through successive reduction and oxygenation reactions in the presence of molecular oxygen and electrons supplied by NADPH (Ryter et al., 2002
1 µM. The promotion of adventitious root development in auxin-depleted cucumber explants was maximal at 10 µM hematin and at 10 µM SNP or 10 µM IAA (data not shown). We also noted that hematin response was greater in comparison with the IAA or SNP effect (
