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First published online October 17, 2008; 10.1104/pp.108.125674 Plant Physiology 148:1985-1995 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
Mechanism of Infection Thread Elongation in Root Hairs of Medicago truncatula and Dynamic Interplay with Associated Rhizobial Colonization1,[W],[OA]Laboratoire des Interactions Plantes Micro-Organismes, UMR CNRS-INRA 2594/441, F–31320 Castanet-Tolosan, France (J.F., A.C.J.T., B.J.S., M.C., D.G.B.); and Institut Fédératif de Recherche 40, Pôle de Biotechnologie Végétale, F–31326 Castanet-Tolosan, France (A.J.)
In temperate legumes, endosymbiotic nitrogen-fixing rhizobia gain access to inner root tissues via a specialized transcellular apoplastic compartment known as the infection thread (IT). To study IT development in living root hairs, a protocol has been established for Medicago truncatula that allows confocal microscopic observations of the intracellular dynamics associated with IT growth. Fluorescent labeling of both the IT envelope (AtPIP2;1-green fluorescent protein) and the host endoplasmic reticulum (green fluorescent protein-HDEL) has revealed that IT growth is a fundamentally discontinuous process and that the variable rate of root hair invagination is reflected in changes in the host cell cytoarchitecture. The concomitant use of fluorescently labeled Sinorhizobium meliloti has further revealed that a bacteria-free zone is frequently present at the growing tip of the IT, thus indicating that bacterial contact is not essential for thread progression. Finally, these in vivo studies have shown that gaps within the bacterial file are a common feature during the early stages of IT development, and that segments of the file are able to slide collectively down the thread. Taken together, these observations lead us to propose that (1) IT growth involves a host-driven cellular mechanism analogous to that described for intracellular infection by arbuscular mycorrhizal fungi; (2) the non-regular growth of the thread is a consequence of the rate-limiting colonization by the infecting rhizobia; and (3) bacterial colonization involves a combination of bacterial cell division and sliding movement within the extracellular matrix of the apoplastic compartment.
Higher plants are able to establish mutually beneficial endosymbiotic interactions with a variety of microorganisms. Among these, two root endosymbioses are of particular agricultural and ecological importance. Glomeromycota fungi are able to associate with the majority of vascular land plants to form so-called arbuscular mycorrhizas (AMs), whereas root nodulation involving nitrogen-fixing soil bacteria of the Rhizobiaceae family is restricted to the legume family. In these tightly regulated biotrophic associations, host-microbe recognition and initial root entry are crucial steps in the establishment of these two endosymbioses, and, in both cases, outer root penetration by the infecting microsymbiont is transcellular, involving the formation of a specialized host membrane/cell wall interface, which physically separates the microbe from the host cytoplasm (for review, see Brewin, 2004  ; Genre and Bonfante, 2005; Parniske, 2008). This process, which involves the formation of an apoplastic compartment within the host cell, has been termed accommodation (Parniske, 2000).
For temperate legumes, such as the model legume Medicago truncatula, rhizobia penetrate the host root through epidermal root hairs. The recognition between host and bacteria is based on the synthesis of specific rhizobial lipo-chitooligosaccharides known as Nod factors (NFs). These signal molecules elicit a number of cellular responses in root hairs as a prelude to infection (e.g. Ca2+ oscillations and tip growth reorientation), as well as divisions in inner cortical cells leading to nodule primordium formation (for review, see Oldroyd and Downie, 2008
Genetic approaches have revealed at least three M. truncatula genes (DMI1, DMI2, and DMI3 [for DOESN'T MAKE INFECTIONS]) whose functions are essential for the establishment of both rhizobial and AM symbioses. The three dmi mutants are totally defective for initial root infection by both endosymbionts (Catoira et al., 2000
Recent in vivo confocal imaging techniques using GFP tagging of cellular components have provided important information about host cell reorganization both prior to and during AM infection (Genre et al., 2005 In this article, we describe experimental techniques that allow direct confocal microscopic observation of fluorescently labeled cellular markers in M. truncatula root hairs to gain insight into the cellular mechanisms involved in IT formation during infection with fluorescently labeled rhizobia. GFP targeting of the host cell ER and the IT membrane has allowed us to investigate the relationships between IT growth, bacterial colonization, and the intracellular dynamics of the root hair. These in vivo data have revealed that IT elongation anticipates bacterial colonization within the thread, indicating that this process is primarily host driven. Furthermore, the growth of the IT appears to be discontinuous, comprising alternating phases of rapid and slower (or temporarily arrested) tip extension. Highly variable IT growth rates are reflected both in the position of the migrating root hair nucleus ahead of the IT tip, as well as in the form of the connecting cytoplasmic bridge. Finally, these observations have revealed that gaps are frequently present within the rhizobial cell file inside the growing IT and have led us to conclude that the colonizing bacteria progress down the newly formed apoplastic compartment by a combination of cell division and collective movement. Based on these findings, we propose a scenario for rhizobial infection of root hairs and compare the cellular mechanism of IT growth with the PPA-based infection process described for intracellular AM infection.
In Vivo Studies of Infection Thread Growth in M. truncatula Root Hairs
To perform confocal microscopy studies of rhizobial infection in M. truncatula root hairs, we have developed an experimental procedure similar to that previously used for AM infection (Genre et al., 2005
Because fluorescence labeling of the ER has proved to be extremely useful for visualizing both the cytoplasmic and nuclear dynamics of the host cell during AM infection (Genre et al., 2005 To distinguish the fluorescence labeling of the bacterial partner in the confocal microscope, composite M. truncatula sunn plants expressing 35S:GFP-HDEL were inoculated with an S. meliloti 2011 strain that stably and constitutively expresses the Cerulean version of the cyan fluorescent protein (cCFP; Sm 2011-cCFP, kindly provided by P. Smit, Wageningen, The Netherlands). We have shown that the fluorescence labeling of this strain is stable throughout infection/nodulation (see "Materials and Methods"). The capacity to follow infection in individual root hairs is illustrated in Figure 1 , which shows progressive IT growth at three time points over a 20-h period imaged both by bright-field and confocal microscopy. The GFP-HDEL-labeled cytoplasmic bridge located between the migrating nucleus and the growing IT is clearly visible in Figure 1C. Note that the position of the root hair nucleus can be deduced from the strong perinuclear ER labeling (Fig. 1C), and also that the IT is surrounded by ER-rich cytoplasm at all stages of development (Fig. 1, C, F, and I).
Having identified growing ITs by this approach, it was then possible to investigate different stages of bacterial colonization in relation to thread development. In mature ITs, which have fully traversed the root hair, the colonizing rhizobia are often in the form of multiple braided files (Supplemental Fig. S1, C and E; Gage, 2002 ). However, Figure 1, B and E, clearly shows that the bacteria close to the growing tip of the IT are aligned in a single file (Dart, 1974), and indeed we have never observed multiple files of rhizobia in the tip region of an actively growing thread. In addition, the images in Figure 1 show that the file of cCFP-labeled bacteria within the growing IT is often interrupted by gaps of variable length. As discussed in more detail later, these gaps within the bacterial file indicate the absence of bacteria rather than the loss of fluorescence (see also "Materials and Methods"). To our surprise, repeated observations of over 30 growing ITs using the GFP-HDEL marker revealed significant variations in growth rate, the shape and diameter of the cytoplasmic bridge, as well as the distance between the IT and the migrating nucleus. To further investigate this variability, and in particular the dynamics of IT elongation and associated bacterial colonization, it was first necessary to identify a fluorescent marker for the newly synthesized tip of the IT compartment. This was of crucial importance because the precise localization of the growing tip region of the IT in either bright-field or confocal images of GFP-HDEL-labeled root hairs is extremely difficult because this region is usually surrounded by dense, ER-rich cytoplasm (e.g. Fig. 1, A and C; Dart, 1974).
As stated earlier, the apoplastic compartment within the IT is separated from the cell cytoplasm by a membrane-extracellular matrix interface, with the matrix lining the inner surface of the thread. The IT membrane is contiguous with the plasma membrane (PM) and is thought to be initiated from within the curled root hair containing rhizobia via the invagination of the PM (Brewin, 2004
Growth of the IT within the root hair is shown in detail in Figure 2, A to D, where the tip has moved approximately 6 µm down the hair shank during the 2.5-h period between the two observations. The labeling of the IT interface reveals that there is a space between the leading cell of the bacterial file and the tip of the growing IT (Fig. 2, B and D). A second infection event is illustrated in Figure 2, E to J, monitored at three time points over a 20-h period. In this case, the leading end of the bacterial file is initially close to the IT tip (Fig. 2, E and F), whereas 3.5 h later, a significant space has been created in front of the bacterial file resulting from IT tip elongation (Fig. 2, G and H). This intriguing observation is dealt with in more detail in the following sections. Whereas the surface of the IT close to the advancing tip has a relatively smooth appearance (Fig. 2, F and H), the same segment of the IT observed 20 h later (Fig. 2J) now possesses a very uneven AtPIP2;1-GFP labeling. In fact, this irregular appearance of the fluorescent labeling is already visible in the older segment of the growing IT at the 3.5-h time point (Fig. 2H), suggesting that this modification occurs at a relatively early stage of IT development. We presume that the irregular contour of the IT interface reflects developmental changes in the underlying extracellular matrix. In conclusion, the AtPIP2;1-GFP tag is an excellent tool for visualizing both IT elongation and developmental changes of the IT interface throughout root hair infection, as well as for studying the relationship between IT elongation and both the intracellular dynamics of the host cell and the colonization of the apoplastic compartment by the microsymbiont. In the following sections, the kinetics of IT development and the dynamic interplay between IT growth and bacterial colonization will be examined in more detail.
In the second infection event illustrated in Figure 2, E to J, the mean growth rate of the IT had been estimated as 12 µm h–1 over the 3.5-h period preceding the initial stage depicted in Figure 2F (data not shown). During the following 3.5-h period (Fig. 2, F and H), the mean extension rate of the IT then dropped to only 2 µm h–1. In spite of this significant reduction in average elongation rate, the IT nevertheless successfully reached the base of the root hair the following day (Fig. 2J). To examine the kinetics of IT tip progression in more detail, two independent experiments were performed using roots of composite sunn plants expressing AtPIP2;1-GFP. Based on a total of eight individual growing ITs observed over periods between 2 and 6 h, we calculated an average tip elongation rate of 4.0 ± 2.5 µm h–1 (n = 19). A similar rate of 5.0 ± 2.0 µm h–1 (n = 9) was estimated for a smaller sample of growing ITs observed in a transgenic wild-type line expressing the GFP-HDEL construction (see "Materials and Methods"). However, it is important to underline that, as in the case of the infection event illustrated in Figure 2, E to J, average growth rates for individual root hairs over 2- to 3-h periods ranged from 1 to 12 µm h–1, and frequently changed during IT elongation. These observations indicate that the rate of IT extension can be highly variable throughout the growth of an individual IT. We therefore asked whether the variability in growth rate of an individual IT could be related to the accompanying intracellular dynamics of the infected root hair and, in particular, to the position of the nucleus relative to the growing IT and the form of the cytoplasmic bridge linking the nucleus to the IT. An analysis of 30 images of root hairs with growing ITs revealed that the distance between the IT and the nucleus can vary from 0 to 40 µm, with an average of 20 ± 10 µm. The rapid changes in nuclear position that can occur during the growth of an individual IT are well illustrated in the time series presented in Supplemental Figure S2. Initially, the nucleus is at a typical distance (approximately 30 µm) from the growing IT and the connecting cytoplasmic bridge is relatively broad (Supplemental Fig. S2C). However, 3 h later, the nucleus has moved away from the growing IT with the cytoplasmic bridge becoming longer and much narrower (Supplemental Fig. S2F). This cytoarchitecture then reverses during the following 3.5 h period with a shortening of the IT-to-nuclear distance and a broadening of the bridge (Supplemental Fig. S2I). Interestingly, the progression of the colonizing bacterial file indicates that IT growth is particularly slow during the initial 3-h period. Although these observations do not allow a precise correlation to be drawn between the IT-to-nuclear distance and the rate of IT extension, it is nevertheless tempting to link the slow progression of the IT over the initial 3-h period to the movement of the nucleus away from the growing invagination and the associated narrowing of the cytoplasmic bridge. In conclusion, confocal observations of growing ITs using fluorescent markers for both the ER and the IT interface indicate that the construction of the apoplastic compartment is a discontinuous process, most probably involving phases of rapid elongation alternating with slow (or pausing) IT extension, and that these phases are likely correlated with changes in intracellular dynamics.
Our in vivo studies of IT growth in M. truncatula root hairs have revealed the presence of bacteria-free spaces of variable length between the IT tip and the leading cell of the bacterial file (Fig. 2). To understand the significance of this in relation to discontinuous IT growth, we examined eight growing ITs at several time points in two independent experiments using sunn composite plants expressing the AtPIP2;1-GFP tag. In approximately 65% of the images (n = 27), we observed a bacteria-free space behind the IT tip ranging in length from 2 to 10 µm, and with an average size of 4.0 ± 2.0 µm (n = 17). In certain cases, as in Figure 2, F and H, large variations in the distance between the IT tip and the bacterial file were observed for the same growing thread at different time points. We therefore deduce that extension of the invagination precedes bacterial colonization of the apoplastic compartment and does not require direct physical contact of the IT tip with the rhizobia. In addition, the discontinuous growth of ITs also appears to be reflected in the variability of the distance between the IT tip and the bacterial file, suggesting that these two parameters may be interrelated.
Gaps within the bacterial file were observed in approximately two-thirds of the elongating ITs in root hairs of both sunn and wild-type plants. In the case of the two infections shown in Figures 1 and 2, E to J, multiple gaps are present within the respective files at the first time point (Figs. 1B and 2E). When the two infection events were observed 3.5 h later, bacteria had multiplied within the IT and several of these gaps had disappeared (Figs. 1E and 2G). Finally, as infection continued down the root hair, new gaps appeared within this upper section of the IT (20-h time point; Figs. 1H and 2I). These observations suggest that the bacteria are able to physically move down the thread and also that cell multiplication can occur elsewhere than at the leading end of the bacterial file behind the IT tip. This is particularly well illustrated in Figure 3
, which shows infection within a root hair of a wild-type M. truncatula plant expressing GFP-HDEL. This time series reveals that, 6 h after initial imaging (Fig. 3C), several short bacterial files of variable length and separated by gaps of variable sizes are present within the IT. Two hours later (Fig. 3E), these files and the accompanying gaps have moved together down the IT and the files have extended their length, presumably resulting from a round of bacterial cell divisions. The high stability of the pHC60-derived plasmid carrying the cCFP marker, illustrated by the recovery of 100% fluorescent S. meliloti colonies from crushed nodules ("Materials and Methods"), argues that these gaps are not composed of rhizobia that have lost their fluorescence. This is supported by the fact that internal bacterial file segments frequently extend to fill preexisting gaps during IT progression (e.g. Fig. 2, E and G). Similar gap formation and filling within the rhizobial file was also observed when we replaced Sm 2011-cCFP by the same strain labeled with GFP (Limpens et al., 2003
In conclusion, bacterial colonization of growing ITs in M. truncatula root hairs involves both bacterial division and the collective movement of bacteria down the thread, and we observe that these events can occur simultaneously and over a significant portion of the IT. The interplay between discontinuous IT growth and the mechanism of rhizobial colonization will be discussed below.
The remarkable cellular process involving the initiation and growth of the tubular intracellular structure known as the IT, which allows the controlled entry of nitrogen-fixing rhizobia into the host legume root, has been the subject of microscopic studies over the last half-century (e.g. Fåhraeus, 1957 ; Nutman, 1959; Dart, 1974; Kijne, 1992; Brewin, 2004; Gage, 2004). With the development of confocal microscopy, it is now possible to examine the intracellular dynamics associated with the elaboration of this specialized apoplastic compartment. In this article, we describe an experimental protocol for performing in vivo confocal studies of rhizobial infection within root hairs of the model legume M. truncatula and the identification of appropriate fluorescent markers, which allow concomitant visualization of the growing IT, the infecting microsymbiont, and various cellular components that play an active role in IT development. The results that have come out of these studies have revealed new information about the process of transcellular IT growth, the complex coordination of IT development with rhizobial colonization, and the mechanism of rhizobial colonization within the IT.
The possibility of following the growth of individual ITs over time and, in particular, the concomitant monitoring of both IT development and rhizobial colonization using fluorescent markers, has revealed a number of important features of this complex process. One of the most striking is the apparent irregularity of IT progression, illustrated most clearly by the highly variable rate of IT growth (ranging from 1–12 µm h–1). This irregularity is reflected both in the variable distance between the nucleus and the growing thread (0–40 µm) and the form of the connecting cytoplasmic bridge (Fig. 3; and Supplemental Fig. S2). These variations have been observed not only between different infection events, but also throughout the growth of individual ITs. It is likely that the IT elongation rate is directly related to the cytoarchitecture of the infected root hair, and we strongly suspect, based on our observations, that a closely positioned nucleus and a broad cytoplasmic bridge are associated with periods of rapid thread extension (Supplemental Fig. S2). Indeed, it is probable that a broad cytoplasmic bridge is necessary for supplying the growing IT tip with sufficient quantities of exo- and endocytotic vesicles required for the assembly of the matrix/membrane components of the thread, similar to the situation described recently for AM infection (Genre et al., 2008 The aquaporin AtPIP2;1-GFP fusion labels the IT membrane within the root hair and thereby enables visualization of the elongating tip of the IT in the confocal microscope (Fig. 2). This is important because the apex of the IT is usually embedded in dense cytoplasm and hence difficult to observe in the light microscope (e.g. Fig. 1A). Concomitant fluorescent labeling of the colonizing bacteria has revealed that the leading rhizobia are generally located at a distance of up to 10 µm from the growing tip (Fig. 2, B, D, and H). This strongly argues that IT growth is a host-driven process that does not require permanent physical contact with the bacteria within the thread. Taken together, our data suggest that IT growth is intermittent, with phases of active tip extension alternating with periods of slow or paused growth. To comprehend the mechanisms underlying this irregularity, it is necessary to first consider the process of bacterial colonization within the progressively extending apoplastic compartment.
We have calculated from our in vivo experiments that the average growth rate for the IT in M. truncatula root hairs is 4.0 ± 2.5 µm h–1. This is similar to the IT growth rate previously estimated for clover (5–8 µm h–1; Fåhraeus, 1957
Because rhizobia lack flagella when inside the thread, Gage and Margolin (2000)
Despite the combination of sliding movement and cell division, bacterial colonization of the IT is likely to be a limiting step in IT growth rate. Indeed, it is striking that bacteria are particularly sparse in recently initiated ITs and in the tip region, in general (e.g. Figs. 1B, and 2, A and F). Furthermore, the average IT growth rate of 4 µm h–1 is only 30% of the maximum extension rate (12 µm h–1) observed in our experiments. We therefore propose that the discontinuity in IT growth within the root hair results from the disparity between the potential tip elongation rate and the limiting speed of bacterial colonization. In such a scenario, IT progression would comprise periods of rapid host-driven tip extension, which creates space in front of the leading bacterial file, alternating with pauses during which the colonizing bacteria fill the space by combining sliding movement and division (see model in Fig. 4
). Presumably, the lumen of this bacteria-free space is composed of secreted matrix material of host origin (Rathbun et al., 2002
Conserved Host Cellular Mechanisms in Endosymbiotic Infection
To what extent can analogies be drawn between the cellular mechanisms involved in the creation of the apoplastic compartments during AM and rhizobial infection? In the case of the AM association, primary root infection by the endosymbiotic fungus involves the assembly of an ER-rich cytoplasmic bridge called the PPA between the site of fungal adhesion on the epidermal cell surface and the transcellular migrating host nucleus (Genre et al., 2005
Biological Materials
In this study, we have primarily used the Medicago truncatula sunn-2 mutant, kindly provided by E.-P. Journet (Toulouse, France; Schnabel et al., 2005
Sinorhizobium meliloti 2011 strains expressing either GFP (Sm 2011-GFP) or the cerulean version of the CFP (Sm 2011-cCFP) were kindly provided by P. Smit (Wageningen, The Netherlands) and propagated on selective TY medium supplemented with 10 µg/mL tetracycline. The Sm 2011-GFP strain (Limpens et al., 2003
For ER labeling in M. truncatula root cells, we used the 35S-GFP-HDEL construct, also known as mgfp4-ER (Haseloff et al., 1997
Surface-sterilized seeds of all M. truncatula lines were germinated on inverted agar plates for 3 d at 8°C in the dark. In the case of A. rhizogenes-mediated transformation of both sunn and A17 lines, seedlings were transferred to agar-Fåhraeus plates (Boisson-Dernier et al., 2001
For in vivo microscopy studies, an experimental setup previously used for monitoring root hair growth for A. rhizogenes-transformed composite plants of M. truncatula (Sieberer et al., 2005
Rhizobial infection sites were imaged using a Leica TCS SP2 AOBS confocal laser-scanning microscope equipped with a long-distance x40 water-immersion objective (HCX Apo L 0.80). The argon laser bands of 458 and 488 nm were used alternatively to excite CFP and GFP, respectively, and a 561-nm diode to observe cell wall autofluorescence. Specific emission windows of 460 to 480 nm, 500 to 540 nm, and 600 to 670 nm were used for CFP, GFP, and autofluorescence signals, which were false-colored in magenta, green and red, respectively. During scanning, the GFP signal and the combined CFP plus autofluorescence signals were acquired alternatively for each line, using the sequential mode. The images shown are maximal projections of selected planes of a z-stack. Images were acquired and projected using Leica confocal software and processed using the Leica CS, ImageJ (http://rsb.info.nih.gov/ij), and Image Pro Plus (Media Cybernetics) software. Distance measurements were carried out using the Leica CS.
The following materials are available in the online version of this article.
We are grateful to P. Smit (Wageningen, The Netherlands) for providing the S. meliloti 2011 strains expressing cCFP and GFP, to D.-T. Luu (Montpellier, France) for providing the AtPIP2;1-GFP fusion for membrane labeling, and to A. Genre (Torino, Italy) for frequent discussions and critical reading of the manuscript. Received July 2, 2008; accepted October 10, 2008; published October 17, 2008.
1 This work was supported by an international program for scientific cooperation, titled "Cellular mechanisms of plant root infection by endosymbiotic soil microbes," of the Centre National de la Recherche Scientifique and by the Institut National de la Recherche Agronomique (postdoctoral grant to B.J.S.).  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.or) is: Joëlle Fournier (joelle.fournier{at}toulouse.inra.fr).
[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.108.125674 * Corresponding author; e-mail david.barker{at}toulouse.inra.fr.
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