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First published online January 28, 2009; 10.1104/pp.108.135160 Plant Physiology 149:1785-1796 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
The Temperature-Sensitive brush Mutant of the Legume Lotus japonicus Reveals a Link between Root Development and Nodule Infection by Rhizobia[C],[W],[OA]University of Munich, 82152 Munich-Martinsried, Germany (M.M.-Y., J.M., N.T., T.M., M.G., A.B., M.P.); Kazusa DNA Research Institute, Kisarazu, Chiba 292–0818, Japan (S.S., S.T.); and John Innes Centre, Norwich NR4 7UH, United Kingdom (J.P., T.L.W.)
The brush mutant of Lotus japonicus exhibits a temperature-dependent impairment in nodule, root, and shoot development. At 26°C, brush formed fewer nodules, most of which were not colonized by rhizobia bacteria. Primary root growth was retarded and the anatomy of the brush root apical meristem revealed distorted cellular organization and reduced cell expansion. Reciprocal grafting of brush with wild-type plants indicated that this genotype only affected the root and that the shoot phenotype was a secondary effect. The root and nodulation phenotype cosegregated as a single Mendelian trait and the BRUSH gene could be mapped to the short arm of chromosome 2. At 18°C, the brush root anatomy was rescued and similar to the wild type, and primary root length, number of infection threads, and nodule formation were partially rescued. Superficially, the brush root phenotype resembled the ethylene-related thick short root syndrome. However, treatment with ethylene inhibitor did not recover the observed phenotypes, although brush primary roots were slightly longer. The defects of brush in root architecture and infection thread development, together with intact nodule architecture and complete absence of symptoms from shoots, suggest that BRUSH affects cellular differentiation in a tissue-dependent way.
Legumes can establish root nodule symbiosis (RNS) with rhizobia bacteria, which fix atmospheric nitrogen to ammonium in exchange for carbon and are housed intracellularly within the legume plant root nodule organ (White et al., 2007  ). In the legume Lotus japonicus, the symbiotic interaction with Mesorhizobium loti is initiated at root hair cells. Plant root exudates are sensed by rhizobia and stimulate the bacterial production of Nod factor (NF) signaling molecules (Lerouge et al., 1990). NF perception involves the NF receptors NFR1 and NFR5 and leads to rapid physiological and morphological changes, such as membrane depolarization, a rhythmic oscillation of calcium concentration termed calcium spiking, and cytoskeleton rearrangements resulting in root hair deformation (Ehrhardt et al., 1992, 1996; Heidstra et al., 1994; Timmers, 2008). Upon attachment to the root hair tip, rhizobia are entrapped by a process called root hair curling. From a cavern formed by the curled root hair, a tubular-like plant plasma membrane-derived structure, the infection thread (IT), is formed inside the root hair, into which the rhizobia grow by continuous division (Gage, 2004). In parallel, cortical cell divisions are initiated in the root cortex, leading to the development of a nodule primordium. The IT subsequently grows toward the nodule primordium, penetrates into a cortical cell after a cytoplasmic bridge called the preinfection thread was formed, which determines the growth direction of the IT through the cortical cell. Ultimately, the bacteria are released into the plant cell by a process resembling endocytosis. Inside the plant cell cytosol, the bacteria differentiate into bacteroids and form organelle-like symbiosomes that actively fix atmospheric nitrogen.
Initiation of RNS is strictly controlled by the host plant at the level of both plant-assisted rhizobial invasion of the epidermis-derived root hair cell followed by IT formation and development of a nodule primordium in the root cortex. Several different mutants exhibiting a defect in IT and nodule formation have been described phenotypically so far, and a number of genes required for RNS have been isolated (Oldroyd and Downie, 2008
These findings and many others provide evidence for obvious links between phytohormone signaling in nodule and root development. Meristematic cells proliferate and differentiate into cells of root and shoots. Although the shoot apical meristem and root apical meristem (RAM) are under distinct genetic regulation, they share the same developmental mechanism for maintaining the stem cells in response to environmental cues (Veit, 2004
Other essential factors regulating postembryonic development in plants are plant hormones. The spatiotemporal hormone landscape plays a crucial role in the regulation of nodule positioning and the de novo organogenesis in the root. For example, auxin is involved in cell division control, differentiation of lateral roots, as well as in nodule formation (de Billy et al., 2001 The genetic analysis of intersections between general plant development and nodulation requires the analysis of mutants that are not specifically defective in symbiosis, but show pleiotropic developmental defects. Here, we describe the novel nodulation-deficient L. japonicus mutant brush. A detailed phenotypic analysis indicated that root growth and bacterial infection were hampered. BRUSH is thus not a symbiosis-specific gene, but is also required for proper root development. Pleiotropic mutants like brush are invaluable tools to identify the involvement of general plant developmental pathways in nodulation, including hormone regulation. Surprisingly, although root nodule organogenesis was delayed and most nodules were empty, nodule architecture was not affected as such. brush reveals a novel link between cell differentiation specifically in the RAM and rhizobial infection.
L. japonicus brush Mutants Exhibit Nodulation and Growth Defects
Line SL0979-2 was isolated as a nodulation-deficient ethyl methanesulfonate mutant of L. japonicus accession Gifu (referred to as wild type; Perry et al., 2003
In addition to the nodulation deficiency, brush mutants had shorter shoots, shorter primary roots, and red hypocotyls probably due to anthocyanin accumulation (Fig. 1A). The diameter of primary roots was not uniform throughout the length and overall thicker than wild type (Fig. 1, B and C). The number of lateral roots formed on a primary root varied between plants, but, like the primary roots, they were also relatively short (Fig. 1A). Root hairs as well as trichome structure appeared normal (Supplemental Fig. S1B; data not shown). Closer observation of mutant root tips showed that the root apical region was thicker and root hair density was higher (Fig. 1, H and I). Because of the increased root hair density around the root tip, we named the mutant brush. All of the nonsymbiotic aspects of the root phenotype were independent of inoculation with M. loti.
The three different phenotypes (short root, short shoot, and impaired nodulation) described for the brush mutant plants were stably inherited in M4 and M5 generations. All F1 progeny of crosses between L. japonicus accession Miyakojima (MG-20) and one M4 individual of L. japonicus Gifu brush (internal ZopRA database entry J6900) showed normal plant growth and nodule formation, indicating that the brush mutation is recessive. We analyzed 902 self-progeny of these F1 individuals for cosegregation of the root and nodulation phenotypes. In all clearly scorable cases, the root and nodulation phenotypes occurred together, indicating cosegregation of both traits. We observed 688 (76.3%) wild-type plants and 213 (23.6%) plants mutant for both the nodule and the root phenotype. This suggests that a single locus mutation is responsible for the observed defects. The segregation of phenotypes was also analyzed within the self-progeny of four back-cross individuals (BC1) resulting from two independent back-crosses of brush with Gifu wild type. The observed segregation ratio was 74:24 (wild type:brush), with clear cosegregation of root and nodule phenotype. Analysis of molecular markers in mutant F2 individuals derived from the MG-20/brush crosses linked the mutant locus to marker TM0312 on the short arm of chromosome 2 (Fig. 2 ). We identified a total of five mutant recombinants within an interval of <0.1 cM around brush, all of which showed both low nodulation and short roots. Therefore, we concluded that all mutant phenotypes were caused by a single mutation or very tightly linked mutations.
The Nodulation Deficiency of brush Is Temperature Dependent Because initial experiments indicated a temperature dependence of the brush phenotype, plants were subsequently grown at 18°C and 26°C as permissive and restrictive temperatures, respectively. Inoculation with M. loti MAFF 303099 constitutively expressing the DsRed fluorescent protein (MAFF DsRed) allowed us to follow rhizobial infection by fluorescence microscopy. At 26°C, brush mutants formed fewer nodules than wild type (Fig. 1, B and C). Whereas wild-type plants had on average 18 nodules and nodule primordia per root, brush mutants had only two (Fig. 3G ). Of these, only 15% were infected by bacteria compared to almost 100% in the wild type (Fig. 3I). Although root hair curling appeared normal in brush roots, the number of ITs in brush was reduced compared to wild type (Fig. 3H). Most of the ITs showed abortion within the root hair cells and only very few reached the next cell layer (Supplemental Fig. S3). In wild-type roots, nodule primordia were round and infected as seen by the bacteria-derived red fluorescence (Fig. 1, D and E), whereas brush mutant roots mostly developed irregularly shaped, bump-like structures without visible signs of infection (Figs. 1, F and G, and 3, A–C).
Microscopic analysis of sections of nodules and nodule primordia revealed additional brush phenotypes. In wild type, most nodules displayed a brownish color, suggesting bacterial presence and functional nodules (Fig. 1J). In brush mutants, only few nodules showed brownish bacteria-containing cells (Fig. 1K). The overall structure of these mature nodules, including vascular bundles and the central tissue, appeared normal when compared to wild-type nodules under both permissive and restrictive conditions (Fig. 1, J and K). However, the majority of nodules on brush plants did not contain brownish cells, but still showed clear signs of normal organ differentiation (Fig. 1, L and M). These nodules appeared arrested in development as can be seen by the incomplete differentiation of vascular bundles, most likely due to lack of bacterial infection (Fig. 1, L and M; arrow). On the other hand, when brush mutants were incubated at 18°C, most nodules resembled those of the wild type. The brownish color was more pronounced in those nodules, and also the vascular bundle surrounded the nodule central tissue as found in wild-type nodules (Fig. 3, D [arrows] and E). After growth at 18°C, a strong bacteria-derived fluorescent signal was observed within nodule primordia and white immature nodules (Fig. 3F), indicating that these not fully mature structures also were infected by rhizobia. The number of ITs on brush roots also increased at 18°C compared to 26°C, although this increase was not statistically significant and occurred to a similar extent in wild-type plants (Fig. 3H). Wild-type plants grown at 18°C developed fewer nodules and primordia compared to plants grown at 26°C (Fig. 3G). In contrast, brush plants showed a significantly increased number of nodules and primordia at 18°C compared to 26°C. Nevertheless, no full rescue of nodule number up to wild-type level was observed (Fig. 3G). However, at 18°C, the proportion of infected nodules and primordia in brush rose almost 6-fold to 86% (Fig. 3I), indicating that the rhizobial infection process in brush benefits strongly from growth at the lower temperature.
Due to the temperature sensitivity of the symbiotic phenotype, we asked whether the brush primary root growth defect was also rescued at lower temperatures. brush primary roots were longer at 18°C than at 26°C, but not fully restored to wild-type level (Fig. 4A ). Thin sections of roots were analyzed to assess their cellular organization. At 26°C, wild-type roots displayed distinctive and organized cell layers (Fig. 4B). At the meristematic region, called root initial, the putative quiescent center was surrounded by small, actively dividing cells, which later differentiate in the different cell types (Fig. 4B; arrowhead; Supplemental Fig. S4, B and D). These small cells at or near the root initial were filled with cytoplasm, whereas small vacuoles were visible in maturing cells located at the upper distal part of the root initial where cell expansion had occurred (Fig. 4B; arrow). In addition, the root cap region (columella), required for root tip protection, showed uniformly squared, highly enlarged, and longitudinally expanded cells outward in the direction of growth (Fig. 4B; Supplemental Fig. S4, B and D). At the root hair initiation region, all cells were already fully vacuolated and had a regular and longitudinally expanded shape (Fig. 4B; Supplemental Fig. S5A). Epidermal cells were about one-half the diameter of cortical cells and, within each cell layer, cell size was uniform (Supplemental Fig. S5, A and B).
In contrast, in root sections of brush grown at 26°C, a distorted organization within the root cell layers with irregularly filed cells was observed (Fig. 4C; Supplemental Figs. S4, E–H, and S5, C and D). Around the root initials, supernumerous cells were present in which vacuolation had already occurred (Fig. 4C; arrowhead). Moreover, the columella cells in brush showed no longitudinal expansion (Fig. 4C; Supplemental Fig. S4, F and H). In the root hair region, differentiation into vascular, endodermal, and cortical cell layers was observed, but cells were irregularly shaped and aligned (Supplemental Fig. S5, C and D). A strong effect of brush was apparent in the epidermal cell layer, which was not well defined. brush epidermal cells appeared much larger than wild type and were radially expanded. Collectively, these developmental defects gave rise to a severely distorted overall root architecture. Wild-type roots grown at 18°C showed no structural differences to roots grown at 26°C, although the overall root length was shorter (Fig. 4, A–D). Surprisingly, at 18°C, brush mutant roots showed complete restoration of cellular structure, shape, and size to wild-type levels (Fig. 4, C and E; Supplemental Figs. S4, I–L, and S5, E and F). The putative quiescent center at the root initial became distinctive and the small cells at the surrounding area were filled with cytoplasm and without visible vacuoles. The cells were lined up and underwent cellular expansion, resembling the cell expansion zone of the wild type. The longitudinal root columella cell elongation was restored as well and fully expanded outward (Fig. 4E; Supplemental Fig. S4F). Also, in the root hair region, cells expanded longitudinally similar to wild type (Supplemental Fig. S5E). Transverse sectioning revealed that cell shapes and positions in all cell layers were wild type-like (Supplemental Fig. S5F). This analysis revealed that the root phenotype of brush is strongly temperature dependent. The root phenotypes were independent of inoculation with M. loti (data not shown).
To examine whether the brush mutant phenotypes were determined by shoot or root genotype, we performed grafting experiments between brush and wild-type plants. Two weeks after grafting, the roots were inoculated with M. loti MAFF 303099 and nodule formation was analyzed after 4 weeks at 26°C. When wild type as a rootstock was grafted with brush as a scion (wild type/brush), brush shoots grew normal, as did the wild type/wild type grafted plants (Fig. 5, A–C ). However, when stock brush was grafted with wild-type scion (brush/wild type), the shoots looked pale and stunted even 4 weeks after inoculation, probably due to the lack of nodulation of the brush roots. This was similar to the situation in brush/brush grafted plants, which were stunted and non-nodulating (Fig. 5, A–D). On wild-type/brush plants, almost the same nodule number was observed as on wild-type/wild-type roots (Fig. 5D), indicating that the brush phenotype is root autonomous and determined by the root genotype.
The brush Phenotype Is Independent of Ethylene, Abscisic Acid, and GA
The brush mutant phenotypes might be due to a difference in production or perception of the plant hormone ethylene, which was found to be a negative regulator of root growth (Ortega-Martinez et al., 2007
Because the inhibition of primary root growth in brush could be caused by excessive endogenous ethylene production, we applied aminoethoxyvinylglycine (AVG), an ethylene synthesis inhibitor, at different concentrations to reduce the endogenous ethylene level. Application of more than 1 µM AVG caused retardation of root growth in both wild type and brush (data not shown). Below that concentration, in wild type as well as brush plants, root growth was enhanced by the treatment in a dose-dependent manner, although mutant root lengths never reached wild-type levels (Fig. 6B). Thin sectioning of the RAM revealed that AVG treatment did not restore the mutant root architecture back to wild type (Supplemental Fig. S6). We also tested whether the brush nodulation defect could be restored by AVG. The different doses of AVG enhanced nodulation in both wild type and brush in a similar way, but no apparent recovery of the mutant phenotype to wild-type levels of fully colonized mature nodules was observed (Fig. 6C). We obtained similar results upon silver ion (Ag+) treatment (Supplemental Fig. S7), which interferes with ethylene perception (Rodriguez et al., 1999 ).
Other pathways that might be potentially disturbed in brush and responsible for the root growth phenotype are abscisic acid (ABA) signaling, exemplified by the M. truncatula latd short root mutant (Liang et al., 2007 The short root phenotype could also be a consequence of a generally impaired nutritional status. To test this, plants were grown on agar plates containing 1%, 2%, or 4% Suc. Root growth increased in both wild-type and brush plants upon addition of Suc in a dose-dependent manner, but mutant root length was never restored to wild-type levels (Fig. 6D) and the root architecture remained disturbed (data not shown). Treatment of roots with 1% mannitol, which influences osmotic regulation, did not enhance growth of either wild-type or brush roots (data not shown).
Auxins stimulate cell differentiation, number of lateral roots, and nodule formation (Aloni et al., 2006
BRUSH Defines a Genetic Link between Cell Differentiation at the RAM and Rhizobial Infection In this study, we performed a detailed phenotypic analysis of the L. japonicus brush mutant, which exhibited three distinctive phenotypes: short root, short shoot, and low number of nodules. Importantly, the majority of nodules were lacking rhizobial infection. We found that the short root phenotype was caused by a severe distortion of the root architecture. brush root cells failed to elongate properly and to organize into single files that make up the typical root structure. Interestingly, this differentiation defect was specific for the root. Although rhizobial infection and the frequency of nodule formation were suppressed, the overall architecture of the nodule primordia in brush was wild type-like, indicating that cortical cell division and differentiation were not affected. This points to a specific defect that only affects the root architecture, not the initiation of nodule primordia. During microscopic analysis of the brush root apical region, the typical root cell layers could still be distinguished, but longitudinal cellular expansion was disturbed. Moreover, grafting experiments revealed that shoot growth could be restored by replacement of mutant with wild-type roots, suggesting that the shoot phenotype is a secondary effect of the root phenotype. We conclude that brush exerts a specific effect on cell expansion in the root. Moreover, we could pinpoint the symbiotic defect of brush to the infection of the nodule tissue by rhizobia. These specific defects in brush reveal a novel link between cellular development at the root and bacterial infection.
The brush mutant phenotypes were temperature sensitive: at lower temperatures, root architecture, nodule number, and rhizobial infection were improved. In legumes, several temperature-sensitive mutants have been isolated, such as sym5 in pea (Fearn and LaRue, 1991a
Thin sectioning of primary roots of brush revealed aberrant root architecture (Fig. 4, B–E). It has been shown previously that growth in the presence of Suc affects the size of the quiescent center (Feldman and Torrey, 1975
In legumes, rearrangement of the MT is essential for root hair curling, IT formation, and the reentrance into mitosis of cortical cells at the incipient nodule primordium (Timmers, 2008
It is known that plant phytohormones play an important role in plant growth and nodulation. It has been suggested that ethylene directly suppresses cell division in the quiescent center of the RAM, resulting in retarded primary root growth (Ortega-Martinez et al., 2007
It has also been suggested that other hormones such as GA and ABA contribute the root elongation and plant growth (Liang et al., 2007
It has been suggested that gene functions required for nodule formation are recruited from plant developmental pathways (Szczyglowski and Amyot, 2003
Bacterial Growth and Inoculum Preparation
Mesorhizobium loti MAFF 303099 was obtained from the Ministry of Agriculture, Forestry and Fisheries, National Institute of Agrobiological Sciences, Japan. M. loti MAFF 303099 harboring a DsRed, referred to as M. loti MAFF DsRed (kindly provided by Dr. M. Hayashi), and wild-type M. loti MAFF 303099 strains have been used as rhizobial inoculum for nodulation assays, as well as in root hair deformation analyses. In brief, rhizobia were cultured with TY liquid medium and incubated 2 d in a shaker at 28°C. Rhizobia were then washed with double distilled water three times and suspended in half-strength Broughton & Dilworth (B & D) medium (Broughton and Dilworth, 1971
brush mutant plants were obtained from a population of ethyl methanesulfonate-mutagenized seeds of Lotus japonicus B-129 accession Gifu (Perry et al., 2003 Seeds were germinated upon scarification using sand paper, surface sterilization with 2% (w/v) NaClO for 6 min, and subsequent washing with sterile water, to be finally incubated in water at room temperature for 6 h to overnight, depending on the water absorption of the seeds. Germinated seeds were transferred to 1% (w/v) Bacto agar (GIBCO) prepared in rectangular (18 cm x 18 cm) petri dishes completely wrapped with aluminum foil and incubated in vitro at 16/8-h photoperiods for 2 d, and subsequently subjected to 16/8-h photoperiods for another 2 d without wrapping. For experiments in glass jars, plants were transferred to autoclaved 1-L Weckglass jars containing 250 mL of Seramis (Mars GmbH) and 100 mL of half-strength B & D medium with 100 µM KNO3. For nodulation analysis, the medium contained rhizobial inoculum to a final OD600 of 0.001. Pots were sealed with gas-permeable 3M Micropore surgical tape. Plants were collected 1 month after treatment unless otherwise stated in the text. Nodule images were taken using a Leica MZ 16FA (Leica); for fluorescence microscopy, an RFP filter was used. For experiments on agar plates, plants were grown in petri dishes containing half-strength B5 plant growth medium (Sigma) in 1% Bacto agar (referred to as "half-strength B5 agar plates" in the text). This medium was supplemented with different hormones or other molecules as indicated in the text.
All plants were germinated and planted in sterilized pots as described above. Temperature effects were analyzed by incubation of plants in a temperature-controlled growth chamber with a constant temperature of 26°C or 18°C, with 16/8-h photoperiods.
Grafting experiments were carried out as described by Nishimura et al. (2002).
For triple response analysis, plants were germinated as described above. Two-day-old seedlings were transferred to a half-strength B5 Bacto agar plate containing ACC and incubated at 26°C in the dark for an additional 4 d. For analysis of AVG effects on nodulation and root length, a 10,000x concentrated stock of (S)-trans-2-amino-4-(2-aminoethoxy)-3-butenoic acid hydrochloride (Sigma-Aldrich) was prepared in water and then diluted to the final concentration in the medium supplied to each glass jar. The root length was measured from the junction of hypocotyl and root to the tip of the primary root with digital caliper. Plants were incubated in a growth chamber at 26°C or 18°C with 16/8-h photoperiods. For seedling growth in the presence of Suc, 2-d-old plants were transferred to concentrations of 1%, 2%, and 4% (w/v) Suc in half-strength B5 Bacto agar. The plates were covered up to the plant hypocotyls with a sheet of black paper to avoid direct illumination of the roots. The initial positions of the root tips were marked on the plate. Plates were placed in an upright position and root length was measured from the initial mark to the tip of the primary root.
All plants were germinated and planted in glass jars as described above. 1,000x concentrated stocks of NAA (Sigma-Aldrich) and TIBA (Sigma-Aldrich) were freshly diluted in ethanol and added directly to the liquid medium. Because TIBA inhibits lateral root formation, 2% Suc was added in these experiments to maximize lateral root formation.
Nodule sections were examined by bright-field microscopy. For this, nodules were freshly harvested and vacuum infiltrated for 20 min with fixation solution (phosphate-buffered saline buffer containing 2.5% [v/v] glutaraldehyde; Sigma-Aldrich) and left at room temperature for about 1 h. Samples were subsequently embedded in 5% (w/v) agarose in water. Vibratome VT1000S (Leica) was used with settings of 40-µm slice thickness, frequency of 2.0, and vibration speed of 2.0. Sections were mounted to glass slides and analyzed using an Olympus BP50 microscope at 5x objective magnification (Olympus).
For examination of RAM architecture, we used the method described in Tansengco et al. (2003)
brush was crossed with L. japonicus MG-20 accession Miyakojima (Hayashi et al., 2001
All ANOVA and Tukey's honestly significant difference tests were performed with the Vassar statistical homepage provided by Vassar College. (http://faculty.vassar.edu/lowry/VassarStats.html).
The following materials are available in the online version of this article.
This study is a portion of the dissertation submitted by M.M.-Y. to Osaka University as partial Ph.D. thesis requirement. Received January 1, 2009; accepted January 23, 2009; published January 28, 2009.
1 Present address: Ulm University, Institute for General Genetics and Molecular Cytology, James-Franck-Ring, 89069 Ulm, Germany. 
2 Present address: National Institute of Agrobiological Sciences, 2–1–2 Kannondai, Tsukuba, Ibaraki 305–8602, Japan.
3 Present address: Department of Plant Microbe Interactions, Max-Planck-Institute for Plant Breeding Research, Carl-von-Linné Weg 10, 50829 Cologne, Germany. The author responsible for the 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: Martin Parniske (parniske{at}lmu.de).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[W] The online version of this article contains Web-only data.
[OA] Open access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.108.135160 * Corresponding author; e-mail parniske{at}lmu.de.
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