Mediators, genes and signaling in adventitious rooting.
Adventitious roots are post-embryonic roots which arise flora the stem and leaves and from non-pericycle tissues in old roots. It may forms naturally from stem tissue or under stressful environmental conditions; they may also be induced by mechanical damage or following tissue culture regeneration of shoots. There are at least two pathways by which adventitious roots form, or can be induced to form: by direct organogenesis from established cell types such as the cambium; or flora callus tissue following mechanical damage, such as occurs when cuttings are taken. Adventitious rooting (AR) is one of the most important ways of vegetative propagation in plants and one of the most important methods of commercial production of horticultural crops throughout the world. It is a prerequisite for the successful production of viable clones. Because vegetative propagation is frequently practiced by nurserymen for maintaining fidelity and achieving quicker propagation of horticultural and floricultural plants it is necessary to understand the physiological and biochemical basis of AR.
AR follows similar steps and share common mechanisms with lateral root formation (Ermel et al., 2000). It involves a process of redifferentiation, in which predetermined cells switch from their morphogenetic path to act as mother cells for the root primordia. The process of AR consists of three successive but interdependent physiological phases with different requirements, namely: induction, initiation and expression. The induction phase comprises molecular and biochemical events without visible changes. The initiation phase is characterized by cell divisions and root primordia organization. The expression phase is characterized by intra-stem growth of root-primordia and root emergence. For example, the critical events that culminate in the formation of adventitious roots in sunflower hypocotyls, and perhaps some of the other changes, occur within the first 3-12 h after the excision of the original roots (Liu et al., 1990), the first cyclological changes associated with AR primordia are clearly visible at 24 h following derooting in sunflower seedlings, and adventitious root primordia can be seen growing through the epidermis of the hypocotyls within three days after the excision of primary roots (Fabijan et al., 1981b).
Many environmental and endogenous factors, such as temperature, light conditions, hormones (especially auxin), sugars, mineral salts and other molecules, may function as signals and induce groups of cells to redefine their late, resulting in and regulating AR. Phytohormones play complex roles, exerting direct (acting on cell division or cell growth) or indirect (interacting with other molecules or phytohormones) effects. Auxin has been shown to be intimately involved in the process of AR (Wiesmann et al., 1988) and the interdependent physiological stages of the rooting process are associated with changes in endogenous auxin concentrations (Heloir et al., 1996). Several studies have emphasized that polyamines play a role in AR (Biondi et al., 1990; Hausman et al., 1994; Heloir et al., 1996). A possible interrelationship between auxin and polyamines in the control of rooting induction has been suggested by some workers (Hausman et al., 1995). Many studies have reported that ethylene was a signal molecule in AR (Biondi et al., 1990). IAA-induced ethylene production may be a factor involved in the stimulation of AR (Pan et al., 2002). Some of the recent work reported noval signal molecules which involve in AR, such as nitric oxide (NO) (Pagnussat et al., 2002, 2003, 2004), hydrogen peroxide ([H.sub.2][O.sub.2]) (Li et al., 2007) and carbon monoxide (CO) (Xu et al., 2006). It is also known that peroxidase activity regulates IAA catabolism and acts as a marker for the successive phases, typically with a minimum at the induction phase and a maximum at the initiation phase. Great progress has been made in recent years in understanding the auxin response genes and auxin signaling (Parry & Estelle, 2006; Quint & Gray, 2006).
In this review, we focus on AR signaling and responsive genes, and the impressive progress that has been made toward illuminating this fundamental area of plant biology.
Mediators and Signaling Molecules in Adventitious Rooting
Mineral nutrients have essential and specific functions in plant metabolism: they can function as constituents of organic structures, as activators of enzymatic reactions, or as charge carriers and osmoregulators. Nutrition is a key factor determining root morphogenesis through effects on lateral root formation and control of root length and density. Mineral nutrition, i.e. calcium, nitrogen source, zinc, phosphorus, iron and manganese, had an effect on the formation and growth of adventitious roots. Cuttings that were rooted in an optimized mineral nutrient medium showed significantly higher survival after transplanting and drought stress than cuttings rooted in basal medium and treated in the same way (Schwambach et al., 2005). Although AR and mineral nutrition are intimately related, few studies have attempted to characterize the effects of specific minerals on each of the three phases of the rooting process. However, to fully understand the relationship between AR and mineral nutrition, we need to identify the roles of each nutrient in each phase of the rooting process.
Calcium Ion ([Ca.sup.2+])
The calcium ion is now firmly established as a second messenger in numerous plant signaling pathways, conveying a wide range of environmental and developmental stimuli to appropriate physiological responses. Changes in [[[Ca.sup.2+]].sub.eyt] have been reported in response to various signals, including hormones, light, abiotic stress and microbial elicitors. The information encoded in transient [Ca.sup.2+] changes is decoded by an array of [Ca.sup.2+]-binding proteins giving rise to a cascade of downstream effects, including altered protein phosphorylation and gene expression patterns.
To date, the calcium signal in AR is less studied. Bellamine et al. (1998) reported that exogenous [Ca.sup.2+] also seems to affect AR in vitro. The process of rooting was inhibited by the application of calcium chelators and calcium channel blocker. A positive interaction between hormones and specific concentrations of exogenous [Ca.sup.2+] in improving AR was found. Under optimal hormonal and environmental conditions, AR was enhanced by the addition to the medium of a broad range of Ca[Cl.sub.2] (Falasca et al., 2004).
Boric Acid (B)
The micronutrient boric acid (B) caused the development of adventitious roots in sunflower hypocotyl cuttings. In the absence of B, no adventitious roots were formed (Josten & Kutschera, 1999) and root growth of intact plants is rapidly inhibited. This suggests that the micronutrient may be required for the maintenance of cell division, cell enlargement or both of these processes. Experiments with squash plants and cultured tobacco cells that were grown in the absence or presence of boric acid led to the hypothesis that B may play a role as a structural component of the growing (primary) cell walls in developing plant tissues (Hu et al., 1996). In Phaseolus ulgaris or P. aureus, a supply of B is essential for root development in stem cuttings of lightgrown seedlings (Ali & Jarvis, 1988). Jarvis and Booth (1981) proposed a model of AR in which B may have a role in the control of the level of endogenous auxin. This detailed hypothetical scheme of events that may lead to the formation of lateral roots is largely based on results obtained with mung bean cuttings.
Auxin is the major growth-promoting hormone for the initiation of lateral and adventitious root growth. Numerous authors established that auxin had the ability to promote AR. Indole-3-acetic acid (IAA) is the most abundant endogenous auxin in plants, whereas indole-3-butyric acid (IBA) was only recently found as an endogenous auxin in many species. IBA have a higher root-inducing capacity than IAA, but the response to the type of auxin is also species-dependent. Triiodobenzoic acid, an inhibitor of IAA transport, applied to the top of the hypocotyls lowered the rate of root formation (Fabijan et al., 1981a).
Higher auxin concentrations are required for AR during the induction phase, whereas during the formation phase the phytohormone becomes inhibitory; this profile has been observed in various plant species (De Klerk et al., 1999). Auxin induces cells in the pericycle and parenchyma to dedifferentiate and enter initial cell divisions. Formation of the root primordium itself is no longer dependent on auxin. At high concentrations, auxin inhibits root elongation and stimulates cell differentiation. Simultaneously, cell division in the root meristem and the formation of adventitious and lateral roots are promoted. Lateral root primordia can initiate in the early differentiation zone of the root meristem, bur only grow out in response to endogenous auxin delivered from the shoot (Bhalerao et al., 2002). Exogenous auxin can induce additional lateral roots to form and grow out, and can also promote AR on stems or other tissues. Several gain-of-function iaa mutations affect production of lateral or adventitious roots (Fukaki et al., 2002; Rogg et al., 2001; Tatematsu et al., 2004), but it is not known which AR they target.
Gibberellic acid inhibited, while an inhibitor of gibberellin biosynthesis promoted rooting. Low concentrations of cytokinins increased, but higher levels inhibited primordia formation (Fabijan et al., 1981a).
The simple gas ethylene is a plant hormone that regulates many aspects of growth and development. Many studies have reported that ethylene was a signaling molecule in AR. Wound-induced increase in ethylene, seen within 3 h of production in the cuttings, is a key stimulatory factor in the formation of root primordial. When this increase in ethylene is localized in the lower portion of the hypocotyls, there is a promotion of rooting. On the other hand, higher concentrations in the top of hypocotyls may inhibit rooting (Liu et al., 1990). Application of either auxin or ethylene induces AR in Rumex palustris and Rumex thyrsiflorus plants and that inhibition of auxin transport from the shoot to the rooting zone decreases the number of roots induced by flooding. Ethylene may also enhance the sensitivity to auxins (Visser et al., 1996). In apple, ACC (1-aminocyclopropane-l-carboxylic acid) promoted rooting in well aerated systems such as leaf disks, but was inhibitory in agar-grown cuttings, presumably due to toxic amounts of ethylene accumulated around the basal stem (De Klerk et al., 1999). Ethylene induces acidic peroxidases involved in lignin biosynthesis and cellulases and pectinases that facilitate root emergence through stem tissues (Faivre-Rampant et al., 1998). Ethylene may also promote rooting by stimulating cytokinin catabolism (Bollmark & Eliasson, 1990). However, the importance of ethylene in eucalypt AR was not supported by experiments using an inhibitor of ethylene action in the induction phase (De Klerk et al., 1999). It suggests that some of the important events necessary for AR occur during the first few hours after excision of the original root system, the hypocotyl cells on the first day go through a phase during which primordia production is blocked by endogenous ethylene and on the second day enter a phase during which endogenous ethylene promotes rooting (Fabijan et al., 1981a).
The higher ethylene concentration in soil-flooded plants increases the sensitivity of the root-forming tissues to endogenous indoleacetic acid, thus initiating AR (Lorbiecke & Sauter, 1999). Inhibition of ethylene synthesis in roots also led to a decline in root formation under flooded conditions (Visser et al., 1996).
There are many unresolved questions concerning the possible role of ethylene in AR. Both ethylene and ethephon, an ethylene releasing compound, have been reported to promote (Liu et al., 1990), or to inhibit on AR (Nordstrom & Eliasson, 1984).
Ethylene is induced by high auxin concentrations through the promotion of transcription of ACC synthase gene and may affect rooting responses. Ethylene may affect auxin transport (Suttle, 1988) or influence auxin perception (Bertell et al., 1990). Since the NPA (1-naphthylphtalamic acid) binding site is believed to be part of the auxin efflux carrier machinery and may regulate its activity (Ruegger et al., 1998), this would suggest that ethylene inhibits auxin efflux by reducing the synthesis or localization of the NPA-binding protein. Recently, ethylene has been involved in the root control of nucleotide sugar flux (Seifert et al., 2004), which in turn requires an intact polar auxin transport. Ethylene stimulated rooting by enhancing the increase in auxins. It appears that the IAA-induced ethylene production may be a factor involved in the stimulation of AR (Pan et al., 2002).
Auxin can increase the rate of ethylene biosynthesis (Riov & Yang, 1989) and stimulate the production of ethylene and this correlates with the fact that the ACC synthase4 gene has been found to be an early auxin-induced gene (Abel et al., 1995). Another ACC synthase gene is expressed in root tips (Rodrigues-Pousada et al., 1999) and corresponds in position to that of the auxin maximum in the root (Sabatini et al., 1999). Furthermore, the elongation of roots is inhibited by both auxin and ACC, which raises the possibility that their action, in this case, is via a common mechanism. One candidate for this common mechanism is the auxin transport machinery (Casson & Lindsey, 2003).
The relationship between auxin and ethylene in root development has been illustrated by the fact that a number of mutants have been isolated that show resistance to both. An example is the potential auxin efflux component, AtPIN2, allelic to the ethylene-insensitive root1 (EIR1) (Muller et al., 1998). Similarly axr2 is a dominant mutant that confers resistance to both auxin and ethylene (Wilson et al., 1990).
Differentiation processes depend upon endogenous factors, and growth substances such as auxins and polyamines are believed to play a central role. Polyamines and auxins played major roles during the induction of rooting (Nag et al., 2001). A positive correlation between polyamine accumulation and the initial stage of AR was observed in some woody species like Prunus avium (Biondi et al., 1990), poplar (Hausman et al., 1995), pear (Baraldi et al., 1995) and walnut (Heloir et al., 1996), suggesting that polyamines could be used as markers of the rooting process (Tiburcio et al., 1989). In some cases, however, a decrease in polyamine level, particularly Put, is associated with an increase in rooting rates (Bamldi et al., 1995). The accumulation of Put, resulting from the inhibition of its conversion to Spd by cyclohexylamine (CHA), an inhibitor of spermidine synthase, favoured poplar rooting even in the absence of auxin (Hausman et al., 1997). This suggests that the catabolism of Put to y-aminobutyric acid (GABA) is essential for root formation by poplar shoots in vitro. Putrescine seems to be involved in the inductive phase of the AR process, but it is unable per se to induce AR when supplemented at physiological doses.
The oxidative degradation of polyamines is associated with the development of soybean lateral roots, and that the products, particularly [H.sub.2][O.sub.2], of polyamine oxidation are involved in the development of soybean lateral roots. At any rate, there is clear evidence from in situ studies that increased polyamine synthesis is associated with lateral root formation and mefistematic activity (Su et al., 2006).
Many studies have reported that sugar function as signaling molecules in plant cells. Sucrose, glucose, and fructose stimulate the induction of adventitious roots in Arabidopsis, but mannose doesn't influence this process (Takahashi et al., 2003). Glucose is an important signaling molecule for abscisic acid and ethylene and indirectly for auxin, due to interactions of these phytohormones (Leon & Sheen, 2003); however, this may not be the main effect of this carbohydrate, because the glucose effects were also seen in cuttings that had exogenous IBA supply in ah adequate concentration for some species rooting (Fett-Neto et al., 2001). Nonetheless, an effect of glucose on auxin synthesis/response cannot be ruled out. The antagonistic relationship between glucose and ethylene signaling could have helped root development (De Klerk et al., 1999).
A positive effect of glucose on cutting rhizogenesis was found if this hexose was supplied during the root induction phase, followed by sucrose in the root formation step, especially for Eucalyptus globulus. The same effect was not seen with fructose. The beneficiai effect of glucose in the induction phase on root number was also evident under subopfimal auxin concentrations (Correa et al., 2005). Galactoglucomannan oligosaccharides (GGMOs) in certain concentrations might inhibit rooting and the elongation process dependant on auxin used (Kollarova et al., 2005).
Phenolic compounds, i.e. pyrogallol, catechol, phloroglucinol and femlic acid, are reported to act synergistically with auxin on AR (James & Thurbon, 1981). Phenolics might be playing key role for induction of AR, and phenolic compounds can be used as rooting enhancer in tea plant (Rout, 2006).
Vitamin [D.sub.3] (Vit [D.sub.3]) and Vit [D.sub.3]-1ike substances have been found in various plants (Buehala & Pythoud, 1988). Vitamin D and related substances have been recognized as plant growth substances which, inter alia, promote AR in Populus tremula L. (Pythoud et al., 1986), Vigna radiate (Jarvis & Booth, 1981), The action of Vit D on green cuttings of Populus tremula is characterized by a synergistic effect with IBA (Pythoud et al., 1986; Pythoud & Buchala, 1989), but the mechanisms of the rooting promotion and the synergy is unknown. It was, however, established that after the application of Vit D, or IBA a relationship exists between rhizogenesis and the number of leaves left on the cutting after the treatment, Vit D, has no effect on the basipetal transport of sucrose suggesting that the mechanism may involve IBA (Pythoud et al., 1986). Pythoud et al. (1986) investigated that only 1,25-dihydroxyvitarain D, markedly promoted AR, and this to a lesser extent than vitamin [D.sub.3] itself.
Nitric Oxide (NO) and cGMP
Nitric oxide is a bioactive molecule that has recently emerged as a cellular messenger in numerous physiological processes in plants. Pagnussat et al. demonstrated that NO mediates the auxin response leading the AR. A transient increase in NO concentration was shown to be required and to be part of the molecular events involved in adventitious root development induced by IAA (Pagnussat et al., 2002).
NO operates downstream of IAA promoting adventitious root development through the GC-catalyzed synthesis of cGMP. NO acts as a second messenger in the IAA-mediated pathway that induces AR through the activation of the GC catalyzed synthesis of cGMP. Both NO and cGMP are downstream messengers in the IAA-signaling pathway that promotes AR (Pagnussat et al., 2003).
Hydrogen Peroxide ([H.sub.2][O.sub.2])
We demonstrated that [H.sub.2][O.sub.2] may function as a signal molecule, involving in AR in cucumber. Treatment of cucumber seedling explants after primary roots removal with [H.sub.2][O.sub.2] significantly increased the number and the fresh weight of adventitious roots, however, the inhibition of the production of [H.sub.2][O.sub.2] with the specific inhibitors suppress the AR. A higher concentration of endogenous [H.sub.2][O.sub.2] was detected in seedling explants after the primary roots were removed (Li et al., 2007).
Carbon Monoxide (CO)
CO donor Hematin and gaseous CO aqueous solution induced AR in Phaseolus radiatus hypocotyl cuttings. CO-mediated effect was differently reversed when CO scavenger hemoglobin (Hb), CO specific synthetic inhibitor ZnPPIX, the auxin transport inhibitor NPA and nitric oxide synthase (NOS) inhibitor L-NAME were added with Hematin, respectively. Treatment with CO significantly enhanced NO fluorescence, whereas NO scavenger cPTIO significantly inhibited NO fluorescence induced by CO, indicating that CO induces AR of mung bean seedling probably mediated by NO/NOS pathway (Xu et al., 2006).
Mitogen-Activated Protein Kinase (MAPK)
The mitogen-activated protein kinase transduction cascades are important mediators in signal transmission, connecting the perception of extemal stimuli to cellular responses. MAPKs are involved in signaling various biotic and abiotic stresses, and have been implicated in the regulation of cell cycle and developmental processes. The role of MAPK cascades in auxin signaling has been recently discussed. There are several reports linking phosphorylation to auxin signaling in plants. MAPK activity in Arabidopsis is stimulated by auxin and, interestingly, inhibitors that block MAPK activity abolish auxin induced expression of the auxin-responsive reporter BA3:GUS. This suggests that MAPK activity is somehow regulating auxin-induced gene expression (Mockaitis & Howell, 2000). A MAPK signaling cascade is activated during the AR process induced by IAA in a NO-mediated but cGMP-independent pathway. NO activates at least two different pathways during the induction of AR: cGMP-dependent and cGMP independent that involves a MAPK signaling cascade. The activation of both pathways seems to be required for the development of AR in cucumber since if one of them is blocked (Fig. 1, Pagnussat et al., 2004).
Peroxidase (PODs) and IAA-oxidase
Classical plant peroxidases are heme-containing enzymes that catalyse the oxidation of a diverse group of organic compounds. PODs exist in numerous isoenzymatic forms and are separated into anionic (acidic) and cationic (basic) types according to their isoelectric points. It has been suggested that PODs are involved in growth and development processes.
Changes in peroxidase activity and peroxidase isoform patterns have been proposed as biochemical markers of the successive rooting phases (Metaxas et al., 2004; Rout et al., 2000; Syros et al., 2004). Many studies showed that, in the course of AR, the induction period is characterized by a sharp reduction of POD activity, the initiation phase by an increase and the expression phase by a gradual reduction in POD activity (Hatzilazarou et al., 2006; Metaxas et al., 2004; Rout et al., 2000; Syros et al., 2004). Several authors have observed a positive correlation between POD activity and rooting (Syros et al., 2004; Metaxas et al., 2004). According to them, it appeared that root formation occurred after the cuttings have reached and passed a peak of maximum enzyme activity. This simation has not been observed in cuttings of other plant species, such as lilac (Patience & Alderson, 1987), Populus tremula (Pythoud & Buchala, 1989), oak (San-Jose et al., 1992) and Castanea sativa x C. crenata (Concalves et al., 1998). In these species, a clear relationship between rooting ability of cuttings and POD activity was not well established.
Among the peroxidase isozymes, the cationic peroxidase isozymes were reported to be able to degrade IAA (Gazaryan et al., 1999). Changes in POD activity (mainly due to cationic PODs) influence rooting by IAA catabolism. The endogenous auxin level increases in the IBA-treated mung bean hypocotyls during the AR (Chao et al., 2001). Hausman et al. (1995) and Heloir et al. (1996) also reported that the concentration of free IAA elevated up to peaks in NAA-treated and IBA-treated tissues during the AR.
[FIGURE 1 OMITTED]
The decrease in the activity of cationic peroxidase isozymes was found in the IBA-treated tissues. The increase of IAA content in the IBA-treated soybean hypocotyls may be due to the decrease of the cationic peroxidase activity. The decreased peroxidase transcript is correlated with the reduced cationic peroxidase activity in the IBA-treated tissue. The decreased peroxidase activity is due to the inhibition of the de novo synthesis of the cationic peroxidase isozymes during the AR (Chao et al., 2001). Klotz and Lagrimini (1996) reported that IAA and NAA strongly suppressed peroxidase gene expression through regulating the multiple auxin responsive elements within the peroxidase gene promoter. The activity of anionic peroxidases (PODs) and cationic PODs was significantly inhibited by exogenous NAA during the induction of AR.
Both anionic and cationic PODs might be involved in lignin synthesis in soybean hypocotyls (Chen et al., 2002). Cationic PODs are also involved in the biosynthesis of lignin and suberin (Quiroga et al., 2000). The relationship between POD isoforms and the biosynthesis of lignin has been investigated biochemically and cytochemically in a number of plant species, including tobacco, soybean, zucchini and poplar. Among the inductive and the initiative phase during AR, the process of lignification of the cell wall, catalysed by a particular peroxidase (POD), may occur during rooting (Sato et al., 1993).
The decline of the anionic peroxidase activity is highly correlated with the decrease of the lignin contents in the IBA-treated tissues. The inhibition of the lignification in the IBA-treated soybean hypocotyls may be due to the process of redifferentiation induced by IBA (Chao et al., 2001), and to produce the new root primordia during AR. In any case, the increase of lignin content during rooting is due to the fact that cell wall genesis, inherent to cell division and xylem formation, demands lignification during rhizogenesis. The decline of POD activity in NAA-treated hypocotyls was accompanied by a decrease in lignin content.
Auxin-induced changes in IAA oxidase occur during the rooting processes (Liu et al., 1996). IAA-oxidase activity of IBA-treated cuttings increased slightly as compared to control. The activity was found to decrease during induction and initiation phases and increase during expression phase. The peroxidase activity in IBA-treated cuttings increased up to initiation phase and declined at the expression phase (Rout, 2006).
Genes Responsed for Adventitious Rooting
To date, only a few genes have been identified that are associated with the general process of AR. In one of the earliest studies, Dhindsa et al. (1987) detected changes in the pattern of protein and mRNA accumulation during auxin-induced root formation from mung bean hypocotyl. In another set of studies, auxin treatment was used to detect differential gene expression in loblolly pine, apple, and almond microcuttings (Caboni et al., 1997). Liu et al. (2005) isolated and characterized a novel gene controlling the initiation of AR primordia in rice (Oryza sativa L.). The gene, designated Adventitious rootless1 (ARL1), encodes a protein with a LATERAL ORGAN BOUNDARIES (LOB) domain. It is expressed in lateral and adventitious root primordia, tiller primordia, vascular tissues, scutellum, and young pedicels. ARL1 is a nuclear protein and can form homodimers. ARL1 is an auxin- and ethylene-responsive gene, and the expression pattern ofARL1 in roots parallels auxin distribution. ARL1 is an auxin-responsive factor involved in auxin-mediated cell dedifferentiation, and that it promotes the initial cell division in the pericycle cells adjacent to the peripheral vascular cylinder in the stem (Liu et al., 2005).
VvPRP1 and VvPRP2, that are induced in stem cuttings of grape (Vitis vinifera L.) during rooting. Each of these genes encodes a distinct type of proline-rich protein that is related to different groups of putative cell wall proteins, and their expression is rapidly induced in stem segments within 6 h after severing. Further, each gene's transcript becomes most concentrated in the basal portion of the stem segment in the region of new root formation. Induction of these genes is not significantly enhanced by IAA treatment, and the expression of the VvPRP1 gene, but not the VvPRP2 gene, is wound-inducible. These results suggest that these VvPRP genes play an important role in the initiation of new roots on grape stem cuttings, perhaps by altering the cell wall mechanical properties to enable root emergence (Thomas et al., 2003).
A possible role of VvPRP1 and VvPRP2 in stem cuttings may be to increase the plasticity of the cell walls or its reinforcement thus enabling cells to withstand the mechanical pressure involved in the eruption of the root meristem through the surrounding tissues. A similar function is suggested for the structural cell wall proteins involved in lateral root development. The tobacco hydroxyproline-rich glycoprotein HRGPnt3 is specifically expressed in subsets of the pericycle and endodermal cells from which the lateral root are initiated and is considered to be involved in the hardening of the cell wall at the root tip, providing the mechanical strength required for penetrating through the cortex and epidermis of the main root (Keller & Lamb, 1989). Expression of the soybean hydroxyproline-rich glycoprotein SbHRGP is confined to the epidermal cells of the zone from which the lateral roots emerge and is suggested to be involved in cell wall reformation that may be required for the initiation and development of the lateral root from the parental root (Ahn et al., 1996). Some PRP genes involved in lateral root formation production show positive regulation of mRNA expression by auxin supply (Neuteboom et al., 1999).
Initiation of AR from differentiated cells in tobacco is marked by HRGPnt3 gene expression induced before the first primordial cell division (Vera et al., 1994). Early lateral and adventitious root primordium development in Arabidopsis is characterized by the expression of the Lateral rootprimordium (LRP1) gene, which in lateral roots was shown to be turned off before the emergence of the primordium (Smith & Feodoroff, 1995). The root meristemless (rml) mutants of Arabidopsis are characterized by growth arrest of lateral and adventitious roots at a size of less than 2 rum, and the RML genes may thus be considered as markers for late lateral and adventitious root development, including emergence of the root primordium. The paucity of such data indicates that regulation of secondary root development, including AR, is far from understood (Cheng et al., 1995).
The aberrant lateral rootformation (alf) mutants were identified in a screen to identify mutants affected in the production of lateral roots, alf1-1 has been shown to be allelic to the superroot (surl; Boerjan et al., 1995) and rooty (rty) (King et al., 1995) mutants. Although initial growth of the mutant is similar to the wild-type, alfl-1, rty and surl seedlings begin to show deviations from approximately 3 d post germination. Numerous adventitious roots begin to grow from the hypocotyl, lateral root primordial develop at high frequency, root hairs appear at higher density and root elongation is reduced. Along with defects in apical growth, the phenotype of the mutant resembles that of wild-type seedlings grown in the presence of micromolar amounts of auxin (King et al., 1995).
Auxin Responsive Genes in Adventitious Rooting
Auxin-induced gene expression is categorized into short-term and long-term auxin responses. Long-term responses are characterised by genes which are expressed one or more hours after auxin application and which may continue to increase in expression for a number of hours or even days (Guilfoyle, 1986). The short-terms are used to indicate those genes, which are upregulated, by auxin within a number of minutes (Abel & Theologis, 1996). Some of the genes known to be involved in auxin-induced lateral root formation are long-term response genes. The RSI-1 gene is upregulated 4 h after the application of auxin to tomato roots (Taylor & Scheuring, 1994) while the HRGPnt3 gene is upregulated 6 h after auxin application to tobacco roots (Vera et al., 1994). An auxin induced proteinase inhibitor (ARPI) was isolated, which is upregulated approximately 48 h after auxin treatment of tomato roots (Young et al., 1994). Recently, a cDNA clone encoding a novel 2-oxoacid-dependent dioxygenase (2-ODD) which is upregulated during the early phases of AR in Malus domestica 'Jork 9' has been isolated from IBA induced thin-stem-disc culture. The corresponding gene has been designated AR related oxygenase (ARRO-1) and is represented in the apple genome by a number of distinct gene copies. ARRO-1 is expressed in stem discs that are induced to form root-initials 48 h after the beginning of an auxin treatment (Butler & Gallagher, 1999). The expression profile of ARRO-1 represents a long-term auxin response. Analysis of ARRO-I's expression profile in the primary root of apple seedlings indicates that it is also highly upregulated in the root in response to both IAA and IBA (Butler & Gallagher, 2000). Anatural applied outcome of genetic research into rooting is the use of transgenesis to manipulate the ability of shoot cuttings to form roots. As the ROLB (root loci) gene from Agrobacterium rhizogenes has been found to be the most effective among the ROL genes in promoting root formation, this gene has been applied in genetic transformation to improve AR of some recalcitrant plants (Nilsson et al., 1997). The ROLB gene has successfully been transformed and expressed in apple rootstocks M26 (Welander et al., 1998), M9 (Zhu et al., 2001), Jork 9 (Sedira et al., 2001) and pear rootstock BP10030 (Zhu et al., 2003). The ROLB-transformed plant cells show an increased membrane sensitivity to auxin (Shen et al., 1988) indicating that ROLB's mode of action is related to changes in the auxin perception pathway (Delbarre et al., 1994). It has been shown that the ROLB protein overexpressed in Escherichia coli has tyrosine phosphatase activity, and this protein is localized in the plasma membrane of the transformed plant cells (Filippini et al., 1996). The role of ROLB in promoting rooting is thought to be related to a kinase/phosphatase cascade-mediated signal transduction of auxin. However, the exact mechanism of ROLB induced rooting remains to be clarified.
Recent studies demonstrated that auxin response is regulated by two large protein families: the ARF (auxin response factor) proteins and the Aux/IAA proteins (Overvoorde et al., 2005). The 22 ARF proteins encoded by 22 ARF genes in Arabidopsis genome each contain a conserved DNA binding domain near their N terminus and most also have a dimerization domain near their C terminus that can interact with a corresponding domain in Aux/IAA proteins (Ulmasov et al., 1999). Between these conserved N- and C-terminal domains, ARF proteins have a less conserved middle domain that in some cases can activate transcription (Tiwari et al., 2003). Although the best studied ARF proteins function as transcriptional activators, other members of the family may be repressors (Tiwari et al., 2003). Genetic studies have implicated different ARFs in diverse growth processes including embryogenesis (ARF5/MONPTEROS, ARF17), root (ARF7/NPH4, ARF10, ARF16, ARF19) and floral development (ARF1, ARF2, ARF3/ETT1N, ARF6, ARF8), and senescence (ARF2). Mutations in ARF19 have little effect on their own, but in combination with mutations in NPH4/ARF7, encoding the most closely related AR, they cause several phenotypes including a drastic decrease in lateral and AR and a decrease in leaf cell expansion. These results indicate that auxin induces lateral roots and leaf expansion by activating NPH4/ARF7 and ARF19 (Wilmoth et al., 2005).
Auxin probably activates ARF proteins by regulating turnover of ARF-interacting proteins called Aux/IAAs (Dharmasiri & Estelle, 2004). The ARF proteins are negatively regulated by the Aux/IAA proteins (Tiwari et al., 2003). Arabidopsis has 29 Aux/IAA genes encoding 29 Aux/IAA proteins. Most Aux/IAA proteins have four conserved motifs called I-IV. Motif I is a transcriptional repression domain and can repress auxin gene induction responses (Tiwari et al., 2003). Motif II is recognized by [SCF.sup.TIRI] and probably other closely related E3 ubiquitin ligases. These ubiquitinate Aux/IAAs and target them for turnover, and auxin stimulates this pathway (Kepinski & Leyser, 2004). Motifs III and IV constitute a dimerization domain and can interact with similar motifs in ARF proteins (Ulmasov et al., 1999). Gain-of-function mutations in motif II of several IAA genes stabilize the corresponding protein and affect developmental responses to auxin. In several cases these mutations decrease auxin-induced gene expression (Tatematsu et al., 2004). Lateral root primordia can initiate in the early differentiation zone of the root meristem, but only grow out in response to endogenous auxin delivered from the shoot (Bhalerao et al., 2002). Exogenous auxin can induce additional lateral roots to form and grow out, and can also promote AR on stems or other tissues. Several gain-of-function iaa mutations affect production of lateral or adventitious roots (Fukaki et al., 2002; Rogg et al., 2001; Tatematsu et al., 2004).
Auxin Signaling in Adventitious Rooting
Dramatic progress has been made in recent years in auxin signaling, especially in understanding the ARF family of transcription factors that collaborate with Aux/IAA proteins to repress and derepress auxin-controlled transcription (Parry & Estelle, 2006; Quint & Gray, 2006).
The AUX/IAA proteins do not interact directly with DNA but exert their regulatory activity through ARFs. AUX/IAA proteins, which repress the activity of ARFs, function as negative or positive regulators of gene transcription. ARFs act as monomers to regulate gene transcription, and dimerization of ARFs might potentiate their effects (Tiwari et al., 2003). Under sub-threshold auxin concentrations the Aux/IAA proteins heterodimerize with the ARF transcription factors and repress auxin-inducible gene expression. However, In the presence of high auxin, the F-box protein TRANSPORT RESPONSE1 (TIR1), one type of ubiquitin protein ligases (E3) called SCFTM (Petroski & Deshaies, 2005), binds to the Aux/IAA proteins, resulting in their ubiquitination and degradation, thus derepressing auxin-inducible gene expression. Recent studies revealed that TIR1 is an auxin receptor. TIR1/AFBs are the only auxin receptors in the plant cell (Dharmasiri et al., 2005; Kepinski & Leyser, 2005; Parry & Estelle, 2006; Quint & Gray, 2006). Auxin binds directly to TIR1 and promotes the interaction with the Aux/IAA proteins. TIR1 functions together with at least three other related F-box protein/receptors to mediate the auxin response throughout plant growth and development. The Aux/IAA genes themselves are auxin-inducible. This might represent a negative feedback loop that ensures a transient response, with the nascent Aux/IAA proteins attenuating the signaling pathway as auxin levels fall by restoring repression of the ARF transcription factors (Parry & Estelle, 2006).
Adventitious rooting is one of the most important ways of vegetative propagation in plants. Because it is one of the most important methods of commercial production of horticultural crops throughout the world it is necessary to understand the physiological and biochemical basis of adventitious root formation. Many basic studies on adventitious root formation have been carried out under in vitro and also in vivo conditions to distinguish and delineate the successive phases of adventitious root formation and regulation. Many environmental, such as temperature and light conditions, and endogenous factors regulate AR, such as [Ca.sup.2+], sugars, auxin, polyamines, ethylene, nitric oxide, hydrogen peroxide, carbon monoxide, cGMP and MAPKs. These regulators are thought to function as signaling molecles and mediate auxin signal transduction in AR. To date, the intricate network of these signalings in AR is less well understood.
Auxin has been shown to be intimately involved in the process of AR and function as crucial role in AR. During the past few decades, great progress has been made in elucidating the auxin signaling pathway. Perhaps the most important outstanding question is the identity of the auxin receptor. We need to understand how the large families of AUX/IAA and ARF proteins regulate downstream gene expression. It will be interesting to know how these two groups of proteins act coordinately to regulate a diverse array of genes during the growth and development of plants. Finally, apart from the primary auxin response genes mentioned earlier, we know little about the downstream genes that mediate auxin response. We know little about the AR response genes, this will be an interesting region when genes will be identified and applied in genetic transformation to improve AR of some recalcitrant plants.
Acknowledgement This work was supported by the "Qing Lan" Talent Engineering Funds of Lanzhou Jiaotong University and the National Natural Scienee Foundation of China (30870438 and 30870378)
Published online: 3 April 2009
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Shi-Weng Li (1,3) * Lingui Xue (1) * Shijian Xu (2) * Huyuan Feng (2) * Lizhe An (2)
(1) School of Chemical and Biological Engineering, Lanzhou Jiaotong University, 88 West Anning Road, Lanzhou 730070, Gansu Province, People's Republic of China
(2) School of Life Sciences, Lanzhou University, 222 South Tianshui Road, Lanzhou 730000, Gansu Province, People's Republic of China
(3) Author for Correspondente; e-mail: firstname.lastname@example.org
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|Author:||Li, Shi-Weng; Xue, Lingui; Xu, Shijian; Feng, Huyuan; An, Lizhe|
|Publication:||The Botanical Review|
|Date:||Jun 1, 2009|
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