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First published online February 17, 2006; 10.1104/pp.105.075879 Plant Physiology 140:1494-1506 (2006) © 2006 American Society of Plant Biologists
Defective Long-Distance Auxin Transport Regulation in the Medicago truncatula super numeric nodules Mutant1,[W]Australian Research Council Centre of Excellence for Integrative Legume Research (G.E.v.N., B.G.R., U.M.), Genomic Interactions Group, Research School of Biological Sciences (G.E.v.N., B.G.R.), and School of Biochemistry and Molecular Biology (U.M.), the Australian National University, Canberra, Australian Capitol Territory 0200, Australia; and School of Plant Science, University of Tasmania, Hobart, Tasmania 7001, Australia (J.J.R., J.B.R.)
Long-distance auxin transport was examined in Medicago truncatula and in its supernodulating mutant sunn (super numeric nodules) to investigate the regulation of auxin transport during autoregulation of nodulation (AON). A method was developed to monitor the transport of auxin from the shoot to the root in whole seedlings. Subsequently, the transport was monitored after inoculation of roots with the nodulating symbiont Sinorhizobium meliloti. The sunn mutant showed an increased amount of auxin transported from the shoot to the root compared to the wild type. The auxin transport capacity of excised root segments was similar in wild type and sunn, suggesting that the difference in long-distance auxin transfer between them is due to loading in the shoot. After inoculation, wild-type seedlings showed decreased auxin loading from the shoot to the root; however, the sunn mutant failed to reduce the amount of auxin loaded. The time of reduced auxin loading correlated with the onset of AON. Quantification of endogenous auxin levels at the site of nodule initiation showed that sunn contained three times more auxin than wild type. Inoculation of sunn failed to reduce the level of auxin within 24 h, as was observed in the wild type. We propose a model for the role of auxin during AON of indeterminate legumes: 1) high levels of endogenous auxin are correlated with increased numbers of nodules, 2) inoculation of roots reduces auxin loading from the shoot to the root, and 3) subsequent reduction of auxin levels in the root inhibits further nodule initiation.
Legumes have the ability to form a symbiotic relationship with soil bacteria called rhizobia. This interaction leads to the formation of nitrogen-fixing root nodules, which is a result of an exchange of signals between the symbiotic partners. The initiation of nodules by rhizobia is regulated by lipochitin oligosaccharides (Dénarié et al., 1996  ) and involves the reinitiation of the cell cycle in the cortical and pericycle cells of the host root. In indeterminate legumes, nodules are initiated in the inner cortex, in contrast to determinate legumes, where nodules typically start to develop in outer cortical cells (Hirsch, 1992). The nodule primordia start to differentiate and form a mature nodule that is inhabited by rhizobia. Medicago truncatula and Lotus japonicus have been chosen as model legume plants for the legume-rhizobia interaction forming indeterminate (Barker et al., 1990; Cook, 1999) or determinate nodules (Handberg and Stougaard, 1992; Udvardi et al., 2005), respectively. In most legumes, the initiation of nodules is restricted to a narrow susceptible zone of the root near the zone of emerging root hairs (Bhuvaneswari et al., 1981). The number of nodules is tightly regulated by the host plant and established nodules suppress the formation of new nodules on the same plant (Caetano-Anollés and Bauer, 1988; Caetano-Anollés and Gresshoff, 1991). This mechanism of restricting nodule numbers is called autoregulation of nodulation (AON). In indeterminate legumes, autoregulation blocks the formation of new nodule primordia, whereas in determinate legumes, autoregulation stops already initiated primordia from developing into a nodule (Caetano-Anollés and Gresshoff, 1991). Removal of already established nodules and root tips enables the formation of new nodules (Nutman, 1952; Caetano-Anollés et al., 1991). The number of nodules is also regulated in response to environmental signals, e.g. nitrate (Streeter, 1988) and the plant hormone ethylene (Penmetsa and Cook, 1997).
Several supernodulating mutants, which have lost the ability to autoregulate nodule numbers, have been described. First to be discovered was the supernodulating soybean (Glycine max) nts (nitrate-tolerant supernodulating) mutant (Carroll et al., 1985a
The phytohormone auxin has long been suspected of playing an important role in the initiation and development of nodules, since Thimann (1936)
A number of experiments suggest that rhizobia manipulate auxin transport. The application of synthetic PAT inhibitors, which interfere with the hormone balance in the root, can induce pseudonodule structures on the root (Allen et al., 1953
Since auxin is a plant hormone transported from the shoot to the root, and because it appears to be an important regulator of nodule initiation, it has been suggested that auxin is part of the autoregulation control of nodulation. Gresshoff (1993)
The M. truncatula sunn mutant has a short root phenotype, and expression studies showed that the auxin response gene GH3 was expressed at higher levels in sunn than in the wild type following inoculation with Sinorhizobium meliloti (Penmetsa et al., 2003
Growth Characteristics of Wild-Type and sunn Seedlings
To confirm the supernodulating phenotype of sunn under our growth conditions, we grew wild-type and sunn seedlings on agar plates in the presence and absence of its symbiont, S. meliloti. Seedlings of the sunn mutant grew to approximately 70% of the length of the wild type 4 d after germination. This was due to shorter root and hypocotyl lengths (P < 0.001 and P < 0.05, respectively; Fig. 1A
). Examination of cortical cell length in the mature root zone of 4-d-old seedlings (2 cm from the root tip) showed that sunn cortical cells were only 85% of the wild-type cell length (P < 0.001; Fig. 1B). Inoculated roots of wild-type seedlings formed an average number of seven nodules per root, whereas sunn seedlings formed an average of 26 nodules per root within 3 weeks after inoculation (Fig. 1C). These results were similar to those reported previously for sunn (Penmetsa et al., 2003
Time Point of AON
To determine the time point at which the autoregulation signal starts to inhibit nodule formation, wild-type plants were inoculated with S. meliloti, and the position of the root tip was marked. New nodule numbers on the primary root were significantly reduced (P < 0.001) in the root segment corresponding to the time point between 24 and 48 h, and 48 and 72 h after inoculation, as compared to the 0- to 24-h segment (Fig. 1D). Beyond the 72-h time point, more nodules were formed. However, these later nodules were spread out along the root (data not shown). These results show that nodule formation is inhibited most strongly from 24 h after initial inoculation of the seedling roots; however, some nodules can be formed afterward. In sunn, a reduction in nodule numbers was also observed at the same time points as in the wild type (P < 0.001; Fig. 1D), although this reduction in numbers was not as pronounced as in the wild type. These results agree with observations by Penmetsa et al. (2003)
To test whether auxin is directly involved in nodulation, plants were grown on the known auxin action inhibitor, p-chlorophenoxyisobutyric acid (PCIB; Oono et al., 2003
When plants were grown on plates containing either the auxin transport inhibitor, NPA, or the auxins IAA, NAA, or 2,4-D at concentrations between 10–5 and 10–7 M (10–8 M for NPA), there were no significant differences in the relative growth rate of the roots between wild type and sunn. In both cases, root growth was inhibited with increasing concentrations of NPA or auxins (data not shown). Nodule numbers also decreased with increasing NPA concentrations; however, the relative inhibition of nodule numbers in sunn was significantly greater than in wild type (Fig. 2B). In response to added auxins, at higher concentrations, nodule numbers decreased similarly in sunn and wild type. However, some low concentrations of IAA (below 10–8 M) promoted nodulation in the wild type (Supplemental Fig. 1; data not shown). When NPA was applied locally just below the cotyledons to reduce auxin transfer from shoot to root, nodule numbers in the wild type were not significantly reduced, but sunn showed a significant (P < 0.001) reduction in nodule numbers (Fig. 3 ). The reduction in nodule initiation was evident both before and after 48 h after inoculation.
Long-Distance Auxin Transport Measurements
To measure the PAT from the shoot to the root (long-distance auxin transport), we adjusted a method (Beveridge et al., 2000
Comparison of Long-Distance Auxin Transport in Wild Type and sunn Long-distance auxin transport was compared between untreated wild-type and sunn seedlings. Auxin transport was measured at 3, 5, and 7 h after application of [3H]IAA to the shoot apex. In wild-type roots, auxin was transported faster per centimeter of root than in the sunn seedlings (Fig. 4, B and C). The time it took for the maximum amount of the radiolabeled auxin to reach segment 5 of the roots was approximately 5 h in wild type and 7 h in sunn. Considering that the root length of sunn was only 70% of the wild type, the speed of auxin transport compared to the root length was similar in wild type and sunn. However, the total amount of auxin recovered in wild type compared to sunn roots was significantly lower (P < 0.001; Fig. 4D). These results suggest that the main difference in auxin transport between wild type and sunn is the amount of auxin transported from the shoot apex into the roots.
To test if inoculation of the roots had an effect on the long-distance auxin transport, 3-d-old M. truncatula root tips were flood inoculated with S. meliloti, and radiolabeled auxin was applied 1, 24, 48, and 72 h after inoculation. The radiolabeled auxin was then allowed to transport for 3 h. All experiments were repeated at least three times on different days with 16 to 20 seedlings each. After 1 h of inoculation no significant differences in auxin transport could be found in either the wild-type or sunn seedlings compared to mock-inoculated roots (Fig. 5, A and C ). After 24 h following inoculation, a significant (P < 0.05) reduction of the amount of [3H]IAA transported could be observed in the wild type (Fig. 5B). This reduction of auxin transport after 24 h correlated with the onset of autoregulation. However, the auxin was still transferred with the same speed as in the control roots. There was no consistent reduction in auxin transport after 48 and 72 h (data not shown).
In the sunn mutant, no significant difference in the amount of transported [3H]IAA or auxin transport speed was found in response to inoculation with rhizobia at any time point (Fig. 5D).
To test whether the difference in radiolabeled auxin transported in wild type and sunn was due to a difference in the transport capacity of auxin between the hypocotyl and the root, we measured the amount of auxin transported from a donor block by an excised segment at the hypocotyl-root junction (set up as in Fig. 6, A and B ) in the wild-type and sunn mutant. We found no significant difference in the amount of radioactivity recovered from either root segments (Fig. 6C) or receiver blocks (data not shown) between sunn and wild type. This finding suggests that the difference in the amount of auxin loaded into the root in wild type and sunn is most likely to occur between the shoot apex and the top of the hypocotyl.
Local inhibition of auxin transport by rhizobia has been previously linked to initiation of nodules (Mathesius et al., 1998 ; Boot et al., 1999). To determine the local auxin transport capacity after inoculation, 4-d-old seedlings were spot inoculated with S. meliloti at the susceptible zone near the emerging root hairs (Fig. 6B). The auxin transport capacity was measured by placing a donor block on the excised root segment 1, 6, 12, and 24 h after inoculation and leaving it on the root for 18 h for the auxin to move into the root and receiver block (Fig. 6A). As soon as 1 h after inoculation, the auxin transport capacity was significantly (P < 0.05) reduced in the wild-type and the sunn mutant, both showing an approximately 20% to 30% reduction in auxin transported (Fig. 6B); at 6 h after inoculation, the auxin transport capacity was still reduced in both the wild type and sunn. However, after 12 h of inoculation, no reduction in auxin transport capacity could be detected, and 24 h after inoculation the capacity for auxin transport was increased in the wild type and sunn (data not shown). The exact timing of the start of the reduction in auxin transport capacity and the following events is difficult to determine in this experimental design because of the 18-h time span necessary for the auxin transport measurements. Therefore, the onset of local auxin transport inhibition starts between 1 and 19 h following inoculation. However, the wild type and sunn followed the same trend in the local reduction of auxin transport capacity.
To test whether changes in auxin transport result in changes in auxin concentration in wild-type and sunn roots and shoots, IAA levels were quantified from whole roots and shoots in 4-d-old seedlings. Free endogenous IAA levels were significantly (P < 0.05) higher in the sunn roots and shoots than in the wild-type roots and shoots (Fig. 7A ). Roots were then inoculated in the zone of emerging root hairs with S. meliloti, and after 24 h, a segment of 1-cm length spanning the inoculation site was harvested. At this time point, the harvested segment corresponded to the young mature root zone. Auxin levels decreased significantly (P < 0.05) in the wild type after inoculation (Fig. 7B). In sunn roots, auxin levels in the zone of inoculation were approximately 3 times as high as in the wild type (P < 0.001), but were not significantly reduced after inoculation (Fig. 7B). Shoot auxin levels were not affected in wild type or sunn after inoculation (data not shown).
Is Auxin Involved in Nodulation?
Several reports in the literature suggested that auxin is involved in nodulation, including evidence that nodules contain elevated levels of auxin, that auxin response genes are differentially expressed during nodule initiation, that auxin transport is inhibited by rhizobia, and that auxin transport inhibitors can induce pseudonodules (for review, see Ferguson and Mathesius, 2003
The hypothesis tested in this study was that the sunn phenotype was due to a direct or indirect defect in the regulation of auxin transport. To differentiate between local and long-distance regulation of auxin transport we developed a method to monitor PAT in M. truncatula seedlings. Using this method, we could determine the speed and the total amount of radiolabeled auxin transported from the shoot into and along the root. This is in contrast to previous methods for measuring local auxin transport regulation in legumes, where either auxin responsive genes were used as an indirect measure of auxin localization in the root (Mathesius et al., 1998
Using our long-distance method, we found that the speed of auxin transport was slower in the sunn mutant compared to the wild type (Fig. 4, B and C). However, the cells of sunn roots were shorter than in the wild type (Fig. 1B), and therefore the mutant had more cells per length of root. Since PAT is a cell-to-cell transport, the speed of auxin transport was approximately correlated with the number of cells through which the auxin was transported. Therefore, the relative speed (the time that is needed to get from the shoot to the root tip) was approximately the same as in the wild type. In addition to cell-to-cell PAT, auxin is also thought to travel in the phloem (Woodward and Bartel, 2005
The amount of auxin loaded from the shoot into the root in wild-type seedlings was reduced after 24 h of inoculation with rhizobia, but the auxin was still transferred with the same speed (Fig. 5B). This time point corresponded to the onset of AON (Fig. 1D). The auxin loading and transport in the sunn mutant did not change in response to inoculation (Fig. 5D). Previous experiments showed that rhizobia have a local effect on auxin transport and it was therefore suggested that auxin transport regulation was part of the process leading to nodule initiation (Mathesius et al., 1998
Our results extend our understanding of the role of auxin transport in nodule initiation by showing that auxin transport inhibition by rhizobia is both a local and a long-distance process. Most likely, these two processes are regulated separately, because only the local regulation of auxin transport is effective in sunn, whereas the long-distance control is defective. Therefore, we suggest that the long-distance control involves a change in auxin loading following inoculation and is not related to the formation of nodules initiated within the first 24 h after inoculation. Instead, we suggest that this reduction of auxin loading could be part of the autoregulation control. Three arguments support that hypothesis. One is that sunn, which lacks AON, did not show a reduction in auxin loading; the second is that the time of AON is correlated with the time of reduction of auxin loading 24 h after inoculation in the wild type; the third argument is that application of NPA below the cotyledons inhibited nodule formation in sunn in the zone of the root that is autoregulated in wild type (Fig. 3). In addition, grafting experiments have shown that the autoregulation signal originates in the shoot (Delves et al., 1986
So far, we do not know how auxin loading could be altered by rhizobia. Rhizobia could either have an effect on the PIN protein(s) or could affect flavonoid synthesis or release, which could alter auxin transport (Brown et al., 2001
The most likely involvement of auxin in nodule initiation is its role as a stimulator of cell division (Roudier et al., 2003
The increased auxin levels that we measured in sunn could also explain the reported phenotypes in sunn in the absence of rhizobia. First, root growth and length of cells are reduced in sunn, consistent with the inhibitory effect of high auxin on root growth. Secondly, Penmetsa et al. (2003)
The hypothesis that high auxin levels are necessary to sustain nodulation is in contrast to the auxin burst control hypothesis proposed by Gresshoff (1993
We hypothesize that a local, transient inhibition of auxin transport at the site of nodule initiation is necessary to initiate nodules. This most likely occurs through blocking auxin efflux from cells near the inoculation site, causing auxin to accumulate where nodules are initiated. Subsequently, the first initiation of nodules sends a so-far-unknown signal to the shoot (Gresshoff, 1993
Plant Material and Growth Conditions
Medicago truncatula cv Jemalong genotype A17, which was used as wild-type control, and its derivative sunn mutant were scarified with sandpaper, surface sterilized, first, for 10 min with 6.25% (v/v) hypochlorite and washed six times with sterile water. Second, seeds were sterilized with 200 mg L–1 Augmentin for 6 h at 29°C, washed six times with sterile water, and germinated on plates containing Fåhreaus (F) medium (Fåhreaus, 1957 To measure cell lengths, 4-d-old roots were stained with 0.1% Methylene Blue for 5 min under vacuum, rinsed in water, and a segment of 1-cm length was excised, starting 2 cm from the root tip. The length of five consecutive cells in the first outer cortical layer was measured with a graticule under a stereomicroscope, using at least 10 seedlings per genotype.
To measure the time point of AON, 3-d-old seedlings were inoculated with rhizobia. After inoculation, the root tip was marked with a permanent marker on the back of the petri dish at 0, 24, 48, and 72 h. After 21 d, nodules formed within the root segments corresponding to the different time points were counted.
Auxin transport was measured in 4-d-old seedlings grown on F medium. We applied 12 pmol of [3H]IAA (Amersham Bioscience, specific activity of 850 GBq mmol–1) in 2 µL ethanol between the cotyledons of the seedling. The seedlings were incubated vertically for 3 h and then cut into 5-mm segments (see Fig. 4A) and placed in a scintillation tube with 4.5 mL scintillation fluid (Perkin Elmer). Samples were gently shaken overnight to facilitate extraction before being analyzed in a Beckman LS6500 scintillation counter (Beckman Instruments). To study the effect of an auxin transport inhibitor, NPA was dissolved into methanol and added to melted F agar medium just before pouring the medium into the plates. Seedlings were transferred to F medium containing NPA 18 h before the [3H]IAA was applied.
To determine the extent of metabolism of the transported [3H]IAA, 4-d-old seedlings were supplied with 12 pmol of [3H]IAA and incubated as above. Whole roots of five seedlings were harvested ground in liquid nitrogen and resuspended in 1 mL 80% (v/v) methanol containing 250 mg L–1 butylated hydroxytoluene. The suspension was shaken for 18 h at 4°C as described by Beveridge et al. (2000)
Prior to auxin transport measurements, roots were treated by spot inoculation of rhizobia in the emerging root hairs zone. For spot inoculation, a glass capillary was pulled over a flame, glued to a hypodermic needle, and autoclaved. A small drop of bacteria (OD600 = 0.1) was placed at the zone of emerging root hairs under a microscope. For measurements at the hypocotyl-root junction, seedlings were not inoculated. The [3H]IAA solution, 7.5 µL of 1 mCi mL–1(Amersham Biosciences), was diluted in 30 µL of ethanol and mixed into 1.5 mL of melted 4% agarose (approximately pH 4.8) in a small petri dish. Once solid, the agar was cut into 8-mm3 donor blocks. Each block contained approximately 4 pmol of [3H]IAA. Plant roots were cut 4 mm basipetal from the point of spot inoculation and 4 mm acropetally. The roots or hypocotyl-root segments were then laid on a modified F plate with the basipetal end in contact with a donor block and the acropetal end in contact with a receiver block (empty agar block). The agar blocks were separated from the media by a strip of Parafilm, to prevent diffusion of the [3H]IAA through the agar. The plates were placed vertically in a box and covered with aluminum foil. They were incubated at room temperature for 18 h. The roots were then cut into two 4-mm segments, above and below the point of treatment (or 4 mm from the hypocotyl-root junction, as judged by the pigmentation of the hypocotyl), and the radioactivity in each segment was analyzed as described above (see Fig. 6A).
The roots, shoots, or root segments were frozen and ground in liquid nitrogen. IAA was extracted and their levels quantified using the methods outlined in Jones et al. (2005)
ANOVA, residual maximum likelihood (REML), and Student's t tests were calculated using Genstat for Windows (version 8.0, Rothamsted Agricultural Trust). REML was calculated when the data were unbalanced. LSDs were determined at the 0.05 level.
We thank Christine Beveridge for help with the long-distance auxin transport experiments and comments on the manuscript, Nerida Holdaway and Robyn Overall for help with the local auxin transport assay, Peter Gresshoff for suggesting the AON time point experiments, and Charles Hocart and Elena Gärtner for technical assistance and comments on the manuscript. We also thank Douglas Cook and Julia Frugoli for kindly supplying the sunn seed and for their many discussions on the topic. Received December 20, 2005; returned for revision February 6, 2006; accepted February 14, 2006.
1 This work was supported by the Australian Research Council through the Australian Research Council Centre of Excellence for Integrative Legume Research (grant no. CE0348212).  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: Ulrike Mathesius (ulrike.mathesius{at}anu.edu.au).
[W] The online version of this article contains Web-only data. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.075879. * Corresponding author; e-mail ulrike.mathesius{at}anu.edu.au; fax 61–2–6125–0313.
Allen EK, Allen ON, Newman AS (1953) Pseudonodulation of leguminous plants induced by 2-bromo-3,5-dichlorobenzoic acid. Am J Bot 40: 429–435[CrossRef][Web of Science] Baluska F, Barlow PW, Baskin TI, Chen R, Feldman L, Forde BG, Geisler M, Jernstedt J, Menzel D, Muday GK (2005) What is apical and what is basal in plant root development? Trends Plant Sci 10: 409–411[Medline] Barker DG, Bianchi S, Blondon F, Dattee Y, Duc G, Essad S, Flament P, Gallusci P, Genier G, Guy P (1990) Medicago truncatula, a model plant for studying the molecular genetics of the Rhizobium-legume symbiosis. Plant Mol Biol 8: 40–49 Beveridge CA, Symons GM, Turnbull CGN (2000) Auxin inhibition of decapitation-induced branching is dependent on graft-transmissible signals regulated by genes rms1 and rms2. Plant Physiol 123: 689–697 Bhuvaneswari TV, Bhagwat AA, Bauer WD (1981) Transient susceptibility of root-cells in four common legumes to nodulation by rhizobia. Plant Physiol 68: 1144–1149 Blakeslee JJ, Peer WA, Murphy AS (2005) Auxin transport. Curr Opin Plant Biol 8: 494–500[CrossRef][Web of Science][Medline] Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433: 39–44[CrossRef][Medline] Boot KJM, van Brussel AAN, Tak T, Spaink HP, Kijne JW (1999) Lipochitin oligosaccharides from Rhizobium leguminosarum bv. viciae reduce auxin transport capacity in Vicia sativa subsp nigra roots. Mol Plant Microbe Interact 12: 839–844[CrossRef][Web of Science] Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126: 524–535 Caba JM, Centeno ML, Fernandez B, Gresshoff PM, Ligero F (2000) Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type. Planta 211: 98–104[CrossRef][Web of Science][Medline] Caetano-Anollés G, Bauer WD (1988) Feedback-regulation of nodule formation in alfalfa. Planta 175: 546–557[CrossRef][Web of Science] Caetano-Anollés G, Gresshoff PM (1991) Plant genetic control of nodulation. Annu Rev Microbiol 45: 345–382[CrossRef][Web of Science][Medline] Caetano-Anollés G, Paparozzi ET, Gresshoff PM (1991) Mature nodules and root-tips control nodulation in soybean. J Plant Physiol 137: 389–396 Carroll BJ, McNeil DL, Gresshoff PM (1985a) Isolation and properties of soybean Glycine max merr mutants that nodulate in the presence of high nitrate concentrations. Proc Natl Acad Sci USA 82: 4162–4166 Carroll BJ, McNeil DL, Gresshoff PM (1985b) A supernodulation and nitrate-tolerant symbiotic (nts) soybean mutant. Plant Physiol 78: 34–40 Cook DR (1999) Medicago truncatula: a model in the making! Curr Opin Plant Biol 2: 301–304[CrossRef][Web of Science][Medline] de Billy F, Grosjean C, May S, Bennett M, Cullimore JV (2001) Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol Plant Microbe Interact 14: 267–277[Web of Science][Medline] Delves AC, Mathews A, Day DA, Carter AS, Carroll BJ, Gresshoff PM (1986) Regulation of the soybean-rhizobium nodule symbiosis by shoot and root factors. Plant Physiol 82: 588–590 Dénarié J, Debelle F, Prome JC (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65: 503–535[CrossRef][Web of Science][Medline] Fåhraeus G (1957) The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J Gen Microbiol 16: 374–381 Ferguson BF, Mathesius U (2003) Signaling interactions during nodule development. J Plant Growth Regul 22: 47–72[CrossRef] Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL, et al (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 44: 179–194[CrossRef][Web of Science][Medline] Geldner N, Friml J, Stierhof YD, Jurgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413: 425–428[CrossRef][Medline] Gresshoff PM (1993) Molecular genetic analysis of nodulation genes in soybean. In J Janick, ed, Plant Breeding Reviews, Vol 11. Wiley Publishers, New York, pp 275–318 Handberg K, Stougaard J (1992) Lotus-japonicus, an autogamous, diploid legume species for classical and molecular-genetics. Plant J 2: 487–496[CrossRef][Web of Science] Hirsch AM (1992) Developmental biology of legume nodulation. New Phytol 122: 211–237[CrossRef] Hirsch AM, Bhuvaneswari TV, Torrey JG, Bisseling T (1989) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc Natl Acad Sci USA 86: 1244–1248 Jones S, DeMeo J, Davies N, Noonan S, Ross J (2005) Stems of the Arabidopsis pin1-1 mutant are not deficient in free indole-3-acetic acid. Planta 222: 530–534[CrossRef][Web of Science][Medline] Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, de Bruijn F, et al (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420: 422–426[CrossRef][Medline] Libbenga KR, van Iren F, Bogers RJ, Schraag-Lamers MF (1973) Role of hormones and gradients in initiation of cortex proliferation and nodule formation in Pisum sativum L. Planta 114: 29–39[CrossRef][Web of Science] Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Nonmanly J, Sandberg G (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17: 1090–1104 Lohar DP, VandenBosch KA (2005) Grafting between model legumes demonstrates roles for roots and shoots in determining nodule type and host/rhizobia specificity. J Exp Bot 56: 1643–1650 Mathesius U, Schlaman HRM, Spaink HP, Sautter C, Rolfe BG, Djordjevic MA (1998) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14: 23–34[CrossRef][Web of Science][Medline] Noh B, Murphy AS, Spalding EP (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13: 2441–2454 Nutman PS (1952) Studies on the physiology of nodule formation. 3. Experiments on the excision of root-tips and nodules. Ann Bot (Lond) 16: 79–103 Oono Y, Ooura C, Rahman A, Aspuria ET, Hayashi K, Tanaka A, Uchimiya H (2003) p-Chlorophenoxyisobutyric acid impairs auxin response in Arabidopsis root. Plant Physiol 133: 1135–1147 Pacios-Bras C, Schlaman HRM, Boot K, Admiraal P, Langerak JM, Stougaard J, Spaink HP (2003) Auxin distribution in Lotus japonicus during root nodule development. Plant Mol Biol 52: 1169–1180[CrossRef][Web of Science][Medline] Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275: 527–530 Penmetsa RV, Frugoli JA, Smith LS, Long SR, Cook DR (2003) Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol 131: 998–1008 Roudier F, Fedorova E, Lebris M, Lecomte P, Gyorgyey J, Vaubert D, Horvath G, Abad P, Kondorosi A, Kondorosi E (2003) The Medicago species A2-type cyclin is auxin regulated and involved in meristem formation but dispensable for endoreduplication-associated developmental programs. Plant Physiol 131: 1091–1103 Scheres B, McKhann HI, Zalensky A, Lobler M, Bisseling T, Hirsch AM (1992) The Psenod12 gene is expressed at 2 different sites in Afghanistan pea pseudonodules induced by auxin transport inhibitors. Plant Physiol 100: 1649–1655 Schnabel E, Journet EP, Carvalho-Niebel F, Duc G, Frugoli J (2005) The Medicago truncatula SUNN gene encoding a CLV1-like leucine-rich repeat receptor kinase regulates both nodule number and root length. Plant Mol Biol 58: 809–822[CrossRef][Web of Science][Medline] Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299: 109–112 Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM (2005) A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17: 2230–2242 Streeter J (1988) Inhibition of legume nodule formation and n-2 fixation by nitrate. CRC Crit Rev Plant Sci 7: 1–23 Terasaka K, Blakeslee JJ, Titapiwatanakun B, Peer WA, Bandyopadhyay A, Makam SN, Lee OR, Richards EL, Murphy AS, Sato F, et al (2005) PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell 17: 2922–2939 Thimann KV (1936) On the physiology of the formation of nodules on legumes roots. Proc Natl Acad Sci USA 22: 511–514 Udvardi MK, Tabata S, Parniske M, Stougaard J (2005) Lotus japonicus: legume research in the fast lane. Trends Plant Sci 10: 222–228[CrossRef][Web of Science][Medline] Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot (Lond) 95: 707–735 Wu CF, Dickstein R, Cary AJ, Norris JH (1996) The auxin transport inhibitor N-(1-naphthyl)phthalamic acid elicits pseudonodules on nonnodulating mutants of white sweetclover. Plant Physiol 110: 501–510[Abstract] This article has been cited by other articles:
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