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. 2011 Aug 1;6(8):1154–1161. doi: 10.4161/psb.6.8.15907

The role of ABC transporters in kin recognition in Arabidopsis thaliana

Meredith L Biedrzycki 1,2, Venkatachalam Lakshmannan 1,2, Harsh P Bais 1,2,✉
PMCID: PMC3260713  PMID: 21758011

Abstract

The ability to sense and respond to the surrounding rhizosphere including communications with neighboring plants and microbes is essential for plant survival. Recently, it has been established that several plant species including Arabidopsis thaliana have the ability to recognize rhizospheric neighbors based or their genetic identity. This study investigated the role of ABC transporters in kin recognition in A. thaliana based on previous evidence that root secretions are involved in the kin recognition response and that ABC transporters are responsible for secretion of a number of compounds. Three genes, AtPGP1, AtATH1 and AtATH10, are all implicated to be partially involved in the complex kin recognition response in A. thaliana based on this report. These findings highlight the importance of ABC transporters in understanding root secretions and plant-plant community interactions.

Key words: root biology, rhizosphere, kin recognition, root secretions, Arabidopsis

Introduction

Although the concept of self/nonself recognition in plants had been investigated for some time, recently, the theory of kin recognition in plants has gained attention.1–3 Recently, published findings by Dudley and File,4 supported the concept of kin recognition in Cakile edentula (sea rocket) based on differences in root allocation patterns when the plants where grown in the presence of kin versus strangers. A further study by Murphy and Dudley,5 demonstrated kin recognition in Impatiens pallida by increasing aerial root growth in the presence of strangers versus in the presence of kin, indicating that different species may alter different traits in response to the relatedness of their rhizospheric neighbors. Additional recent experimental studies on kin recognition in plants have generated excitement at the implications of recognition, but have been criticized for potential pitfalls in experimental setups that could invalidate the conclusions.6–9 Although these studies make clear arguments for the notion of kin recognition, they did not propose a mechanism to make this recognition possible. Biedrzycki et al. (2010)10 examined kin recognition in Arabidopsis thaliana and whether ABC transporters may be involved in this process. In this study, plants were grown in liquid media and exposed to their own secretions, or secretions from a kin (from the same mother plant), or stranger (from a different ecotype) plant. It was determined that plants exposed to secretions from stranger plants grew more lateral roots than those exposed to their own secretions or secretions from a kin plant, indicating that A. thaliana does have the ability to recognize kin plants and alter their growth in accordance with this recognition. Additionally, to some plants, a known root secretion inhibitor, sodium orthovanadate, was added. Plants treated with sodium orthovanadate and plants exposed to stranger secretions no longer grew more lateral roots. Therefore, the role of root secretions in kin recognition in A. thaliana has been identified. Contrary to our studies, a recent work has shown competitive ability rather than kinship to have more of an effect on plant growth in A. thaliana accessions.11 In this study, authors using different accessions tested the varying competitive ability in between accessions under the kin and stranger set up. Masclaux et al. (2010)11 observed competitive ability between accessions reflected in terms of decreased fresh weight and silique number under kin and non-kin treatments. Despite the fact that Masclaux et al. (2010)11 did not find any evolutionary benefit in terms of biomass or seed production as a result of A. thaliana plants being grown with kin versus strangers, does not necessarily indicate kin recognition in A. thaliana does not occur. Whether or not kin members behave altruistically, competitively, or neutrally towards each other may be dependent upon whether or not the group is under biotic or abiotic stress at the time of interaction.12 Therefore, the mechanistic and genetic links to decipher kin recognition in any plant systems still needs to be elucidated.

First identified in bacteria, fungi and animals and later in plants, the ABC transporter super-family, is one of the largest protein families known.13,14 Although they can transport a variety of substrates, ABC transporters share a similar structural architecture and function in that they are comprised of two nucleotide binding folds (NBF) which bind and hydrolyze ATP and two transmembrane domains which move substrates across the membranes (one of each respectively for a half-sized transporter).13–19 A large number of full and half-sized ABC transporters have been identified in plants; the A. thaliana sequence has indicated 129 ABC transporter genes which surpasses the numbers in humans and yeast.13,14,20 Factors contributing to the necessity for a high number of ABC transporters in plant species may include, the potential toxicity of secondary metabolites produced by plants and the need to transport these metabolites out of the cytosol into storage or out of the cell and the vulnerability of plants to soil microbes and other neighboring plants in the surrounding rhizosphere due to their lack of mobility requires detoxification mechanisms for potential exposure to xenobiotics.13 Although detoxification may be the most obvious role for plant ABC transporters, they have also been implicated in other plant processes. Leonhardt et al.21,22 observed ABC transporters; specifically AtMRP5 is involved in A. thaliana regulation of potassium and calcium ion channels during studies with guard cell regulation and stomatal opening.14 Further, Sidler et al. (1998)23 have shown that ABC transporters can be involved in plant growth processes when they determined that AtPGP1 controlled hypocotyl elongation under low light conditions. Later both AtPGP1 and AtPGP4 were shown to be involved in auxin transport and distribution in the roots of A. thaliana.24–26

Plant ABC transporters have more recently been shown to be involved in root secretions. Root secretions play a vital role rhizosphere communication in plant-plant and plant-microbe associations.27,28 In order to demonstrate the involvement of ABC transporters in the root secretion process, Loyola-Vargas et al. (2007)29 showed the direct involvement of specific ABC transport inhibitors on secretion of various compounds. A similar study by Badri et al. (2008)20 compared the root secretion profiles of seven ABC transporter mutants in A. thaliana and found the functional link to independent ABC transporter genes to class of compounds in roots secretions. As previously mentioned, ABC transporters have been implicated in involvement in root secretions. Based on the fact that sodium orthovanadate, a known ABC transport inhibitor, blocked the kin recognition signal in the stranger treatment in Biedrzycki et al.10 one may speculate that root secretions in A. thaliana may be at least in part controlled by ABC transporters.20,30 To examine the role of ABC transporters in kin recognition response in A. thaliana we ask the following questions: (1) Do multiple ABC transport inhibitors eliminate the kin recognition response in A. thaliana? (2) Do multiple ABC transport inhibitors differentially effect the gene expression of a subset of ABC transporters? (3) Do TDNA insertion mutants of ABC transporters exhibit loss of function in triggering the kin recognition response?

Results

Effect of different ABC transport inhibitors on secretion of kin recognition cue.

Our previous studies demonstrated that sodium orthovanadate, a general membrane ATPase inhibitor, had the ability to eliminate the kin recognition response in A. thaliana.10 In this study, we examined whether other known plant root secretion ABC transporters with more specific affinities such as verapamil and nefedipine (calcium channel blockers) or quinidine and glibenclamide (potassium channel blockers) would have the same effect in abolition of kin recognition response.29 Indication of the kin recognition response has been shown as an increase in number of lateral roots when A. thaliana ecotype CHA plants were in the presence of stranger (Col-0) root secretions versus their own secretions or secretions from a kin member when grown liquid culture for one week.10 Our results mirror those of Biedrzycki et al.10 in that the control untreated plants, plants exposed to stranger secretions have significantly more lateral roots per plant than those grown in the presence of kin or own root secretions and there is no significant difference between plants exposed to own, kin or stranger secretions when plants are treated with ABC transport inhibitor, sodium orthovanadate (Fig. 1). Our results also show a similar response for the other four ABC transport inhibitors in that they also eliminate the increase in number of lateral roots when plants are exposed to stranger secretions versus own or kin secretions (Fig. 1). Glibenclamide overall increased the number of lateral roots in all the own, kin and stranger treatments compared to untreated plants, however, the trend of eliminating the kin recognition response was the same as in the other ABC transport inhibitors, indicating the involvement of ABC transporters in secretion of kin recognition cues.

Figure 1.

Figure 1

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The 7-d-old seedlings of own, kin and stranger were co-cultured with 3 µM sodium orthovanadate, glibenclamide, quinidine, nefedipine and verapamil. After 7 d of inhibitors and secretion treatment the numbers of lateral roots were counted. Data presented as mean of at least 33 replicates total from two separate trials. Means of common letters are not significantly different at p ≤ 0.05; according to Duncan's Multiple Range Test. Error bar indicates the standard error to mean at 5%.

Effect of different ABC transport inhibitors on primary root allocation.

Our previously published work showed that in the control treatment, seedlings exposed to media containing stranger exudates had more lateral roots than seedlings exposed to kin or own exudates.10 These results clearly indicate that A. thaliana responds differentially to exudates of kin or strangers. Root length for the target sibship showed a different pattern, with the seedlings exposed to own secretions having longer roots than seedlings exposed to kin or stranger secretions, a pattern expected in self/non-self recognition.10

Addition of sodium orthovanadate, a known ABC transporter inhibitor, eliminated the differences in the number of lateral roots produced by the target sibship between the kin and strangers treatments.10 The administration of sodium orthovanadate slightly reduced the primary root length but did not eliminate the difference between seedlings exposed to own secretions and those exposed to kin or stranger secretions.10 To expand our observation that ABC transporter inhibitors target lateral root cues and not the primary roots, primary root length of plants post-exposure to secretions from own, kin or stranger plants with or without the addition of ABC transport inhibitors was measured. In the control and all of the inhibitor treatments, plants exposed to own secretions revealed significantly longer primary roots, whereas plants exposed to secretions other than their own, whether it be a kin or stranger secretions have shorter primary roots (Fig. 2). As with the lateral root growth, glibenclamide did have an effect on the overall primary root length of the treated plants, but the trend was the same as with the other inhibitors as well as with the untreated plants. This indicates that primary root length is not affected by identity of the non-self secretion whether it be kin or stranger and that it is not-controlled by ABC transporters as the trend was not affected by any of the five ABC transporter inhibitors tested.

Figure 2.

Figure 2

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The 7-d-old seedlings of own, kin and stranger were co-cultured with 3 µM sodium orthovanadate, glibenclamide, quinidine, nefedipine and verapamil. After 7 d of inhibitors and secretion treatment primary root length was measured. Data presented as a mean of at least 33 replicates total from two separate trials. Means of common letters are not significantly different at p ≤ 0.05; according to Duncan's Multiple Range Test. Error bar indicates the standard error to mean at 5%.

Specificity of ABC transporter inhibitors on ABC transporter genes.

In order to determine whether the ABC transport inhibitors had any gene specific activity, three ABC transporter genes known to be localized to the root where chosen for expression studies.20 Additionally, these three ABC transporter genes had previously been shown to be involved in secretion of secondary metabolite compounds and were available in homozygous lines.20 The gene expressions levels were compared for AtPGP1, AtATH1 and AtATH10 for root tissues of plants grown in the presence of own, kin or stranger secretions with or without addition of an ABC transporter inhibitor (Fig. 3A–C). Figure 3A shows the expression levels of AtPGP1 significantly increased in the roots of untreated plants exposed to stranger secretions versus those exposed to own or kin secretions (2.6-fold and 2.16-fold respectively), indicating the involvement of AtPGP1 in the kin recognition process. Expression levels of AtPGP1 are not significantly higher in stranger exposed plants in any of the ABC transporter inhibitor treatments; therefore the inhibitors appear to have an effect on the expression of AtPGP1. Figure 3C shows similar results were found for gene expression levels of AtATH10 as AtPGP1 in that expression level of AtATH10 were found to be 1.87-fold higher in roots exposed to stranger secretions than those exposed to own secretions but there is no significant difference in expression of AtATH10 in treatments with inhibitors. Figure 3B, however, shows expression patterns of AtATH1 show a different trend than the previous two genes, where higher gene expression of stranger exposed plants can be seen in untreated, sodium orthovanadate, glibenclamide and nefedipine treated plants (Fig. 3B). Quinidine and verapamil decrease expression of AtATH1 in plants exposed to stranger secretions, but interestingly increase expression plants exposed to kin secretions. Therefore, all three of these ABC transporter genes are not affected by these ABC transporter inhibitors in the same manner.

Figure 3.

Figure 3

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(A–C) Expression analyses of key genes reveal that ABC transporters inhibitors treatments differentially affect expression of ABC transporter genes. The 7-d-old seedlings of own, kin and stranger were co-cultured with 3 µM sodium orthovanadate, glibenclamide, quinidine, nefedipine and verapamil. After 7 d of inhibitors and secretion treatment RNA was isolated. RT-PCR was performed as described in Materials and methods. Expression levels are represented in arbitrary units, taking the value for kin plants in all the inhibitor treatments as equivalent to 1. Data shown as the mean ± SD of the two replicates.

Functional validation of the involvement of ABC transporter in kin recognition cues.

In order to validate the involvement of AtPGP1, AtATH1 and AtATH10 in the kin recognition process, plants that were homozygous TDNA insertion mutants of these respective genes were obtained and CHA plants were exposed to their secretions rather than the normal stranger Col-0 secretions to determine if these mutants lacking the ABC transporters, were unable to produce the secretion necessary for kin recognition. The number of lateral roots and primary root length of CHA plants exposed to own, kin or stranger ABC transporter mutant secretions were determined (Figs. 4 and 5). CHA plants show a similar response when exposed to ABC transporter mutants as with Col-0 plants in that plants exposed to their own secretions have significantly longer primary roots, whereas exposure to any non-self secretion results in a shorter primary root (Fig. 5) CHA plants exposed to secretions from atath1 and atath10 plants however, do not grow more lateral roots, similar to the response as when grown with kin secretions. CHA plants grew an intermediate number of lateral roots when exposed to root secretions from atpgp1 mutants as compared to when exposed to kin and stranger (Col-0) secretions. These results suggest that AtATH1 and AtATH10 may be involved in the kin recognition response and that AtPGP1 may also be marginally involved in the kin recognition response also, but not to the degree as the other two genes.

Figure 4.

Figure 4

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The 7-d-old seedlings of own, kin and stranger (Col-0) and stranger (ABC mutants) were co-cultured for 7 d, at which time lateral roots were counted. Data presented as mean of at least 33 replicates total from two separate trials. Means of common letters are not significantly different at p ≤ 0.05; according to Duncan's Multiple Range Test. Error bar indicates the standard error to mean at 5%.

Figure 5.

Figure 5

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The 7-d-old seedlings of own, kin and stranger (Col-0) and stranger (ABC mutants) were co-cultured for 7 d, at which time the primary root length was measured. Data presented as mean of at least 33 replicates total from two separate trials. Means of common letters are not significantly different at p ≤ 0.05; according to Duncan's Multiple Range Test. Error bar indicates the standard error to mean at 5%.

Discussion

Previous kin recognition studies focused on the interaction and manifestation of the process such as whether or not it was occurring and how it could be quantified in terms of biomass or number of branches or roots etc. This is the first study which targeted to specifically identify genes that may be involved in the kin recognition process in Arabidopsis thaliana. As in our previous reports, primary root length does not seem to play a role in the kin recognition response or be affected by ABC transport inhibitors in A. thaliana. It appears that primary root length maybe a self/non-self response as it was independent of the identity of non-self secretions. Falik et al.31 and Gruntman and Novoplansky,32 suggest the possibility of gradients or oscillating levels of chemicals produced by roots that may allow for a self/non-self recognition rather than a unique chemical cue for individual plants.

Also, as in our previously published study, we showed that sodium orthovanadate eliminated the kin recognition response by decreasing the number of lateral roots on plants exposed to stranger secretions. Here we show that four additional known ABC transporter and root secretion inhibitors also have the same effect. We took the investigation one step further to correlate whether specific inhibitors had any effect on ABC transporter genes. The ABC transporter genes chosen were known to be highly expressed in root cells and were available in homozygous lines, AtPGP1 is found predominately in Stage 3 cells (Stage 1 closest to root tip-Stage 3 furthest from root tip) and atrichoblast tissues, AtATH1 is found in Stage 3 cells primarily in the endodermis and AtATH10 is located also in Stage 3 cells and in lateral root cap tissues.20 Sodium orthovanadate decreased secretion leading to decreased gene expression in the roots exposed to stranger secretions versus roots exposed to own or kin secretions in AtPGP1 and AtATH10 but not AtATH1 as did inhibitors glibenclamide and nefedipine. Quinidine and verapamil were the only two inhibitors to decrease gene expression in roots exposed to stranger secretions versus own or kin secretions in all three ABC transporter genes, AtPGP1, AtATH10 and AtATH1. Additional testing of CHA plants exposed to secretions of the ABC transporters mutants as strangers revealed a loss of function of kin recognition as plants no longer grew more lateral roots as they did with wild type Col-0 roots for the atath1 and atath10 mutants. Plants exposed to the secretions of the atpgp1 mutants had an intermediate number of roots indicating that this gene may play a role but not be primary for the kin recognition response itself.

Plants exposed to all of the inhibitors showed a reduced number lateral roots when exposed to stranger secretions, however, expression of AtATH1 was only decreased in plants treated with quinidine and verapamil. These results indicate that AtPGP1 and AtATH10 may be partially responsible for the signaling, otherwise the difference in root growth would not have occurred in the other treatments if AtATH1 was solely responsible. Likewise, plants exposed to secretions from atpgp1 mutants only showed an intermediate response to the decrease in the number of lateral roots when compared to plants exposed to Col-0 wild type or the other ABC transporter mutant secretions and perhaps may be partially involved in the kin recognition signaling response. AtATH1 expression was downregulated in all of the inhibitor treatments and exposure to atath1 mutant secretions show loss of the kin recognition function, demonstrating that this gene may play a larger role in the whole process than the other ABC transporter mutants in this study however the other two genes do show some level of involvement. Differences in cellular and tissue localization in roots may play a role in the variation in involvement of these genes in root secretion and kin recognition. Previous studies have also shown that root secretion profiles of ABC transporter mutants did show some overlap in missing peaks as compared to wild-type secretion profiles, demonstrating that one transporter can be involved in the secretion of more than one secondary metabolite and that one ABC transporter can be involved in the secretions of a specific phytochemical.20 Therefore, it is possible that the kin recognition signal could be due to more than one compound, controlled by more than one ABC transporter, or that it could be one compound controlled by one of many ABC transporters, maintaining why AtATH1, AtATH10 and AtPGP1 have varying involvement in the kin recognition process.

AtPGP1 has previously been documented to be involved in basipetal auxin transport in roots, hypocotyl growth and herbicide tolerance and is expressed in plant root and shoots.22,25,33,34 AtATH1 (ABCA2) is also expressed in many tissues and known to be linked to photomorphogenesis.35 AtATH10 (ABC1) is expressed throughout the plant and documented to be involved in light signaling between plastids.36 As each of these ABC transporters is located in several different tissue types, it is possible that they have different substrates and functions in each of these tissues. For example the AtABC1 homolog NpABC1 is involved in leaf excretion of plant defense compounds, highlighting the multiple roles possible for these genes.34

As with most plant processes, complex networks of signaling molecules and gene interactions are needed before a given response can occur and it appears that A. thaliana kin recognition is no different. Here we propose the partial involvement of at least three ABC transporter genes in the kin recognition response, isolating their involvement to the secretion process. However, since during the kin recognition response we see changes in lateral root growth, it is possible that many other genes including those regulating auxin and other growth regulators would be involved. Future investigations to determine these genes as well as the kin recognition signal present in the root secretions would further elucidate this budding field of research.

Method and Materials

ABC transporter inhibitor experiment.

Plant growth and measurement methods were repeated and from Biedrzycki et al. (2010)10 A natural A. thaliana accession (ecotype) was collected by Dr. K. Donohue (Harvard University) from a single North American population near the Charles River in Watertown, MA (CHA prefix) and maintained by single seed descent for at least two generations in the lab. The experiments used a selfed family of CHA25 as the target accession and Col-0 seeds procured from Lehle seeds (TX) as the stranger accession. Seeds were surface sterilized with 50% sodium hypochlorite for 3 min then washed twice with sterile ddH2O. CHA seeds required one week storage in a refrigerator for germination. Seeds were sown in low density, approximately 80–100 seeds of a single accession, evenly spaced on Murashige and Skoog37 media (3% sucrose) plates (100 × 15 mm) for 7 d. On the seventh day, under sterile conditions, CHA and Col-0 seedlings were added individually to wells of a 24 well tissue culture plate (85.5 mm × 127.5 mm, BD Falcon NY USA) with 1 mL of MS liquid media per seedling (1% sucrose) with or without 3 µM of either sodium orthovanadate, glibenclamide, quinidine, nefedipine or verapamil. Plates were placed on a rotary shaker (90 rpm) under cool white fluorescent light (45 mmol m−2 s−1) at 25 ± 2°C. The rotary shaker was used to maintain mixing in the solution and so prevent hypoxia. Order of plates on the shaker was re-randomized daily. Inhibitor treatments were imposed for 7 d. Each day for 7 d, target plants in the own treatment were lifted out of their wells gently with forceps and placed back into the well containing their exudates. Target plants in the kin treatment were lifted from their wells gently and placed into a well with media that previously contained a sibling. Target plants in the strangers treatment were lifted out of their wells gently and placed in a well with media that previously contained a stranger plant (Col-0 ecotype).10 In the stranger treatments, each seedling was paired with one other seedling, so that each seedling was only exposed to the exudates of one other seedling, and these two seedlings were switched daily so that they experienced fresh exudates from their partner over the course of the experiment. The own seedlings were lifted and replaced daily to control for handling. All seedlings were maintained under sterile conditions. Seven days after transfer to liquid media, seedlings were removed from the wells and the number of lateral roots and length of primary roots on each plant was determined with the unaided eye and recorded. Approximately 1–3 plants per plate were damaged and therefore not recorded. Experiments were repeated on two separate occasions with a total of at least 33 plants per treatment from the two separate trials.

ABC transporter mutant experiment.

All conditions above except stranger treatment plants were switched to a well that previously contained one of the mutant plants (Atpgp1, Atath1 or Atath10) rather than a wild type Col-0 plant. At the time of root measurements, ABC transporter mutants did not exhibit any observable difference in phenotype as compared to their background Col-0 wild type plants.

RNA isolation and reverse transcription-polymerase chain reaction.

Approximately, 10 mg of roots from each treatment were frozen under liquid nitrogen, and subsequently powdered using a mortar and pestle. Then, total RNA was extracted using RNeasy® mini kit according to the instruction manual (Qiagen, Valencia, CA). Possible contaminant genomic DNA in RNA extract was removed using turbo DNA-free™ kit (Ambion). The concentration of total RNA was determined spectrophotometrically at 260 nm. The integrity of RNA was checked by electrophoresis in formaldehyde denaturing gels stained with ethidium bromide. First-strand complementary DNAs were synthesized from 0.5 µg of total RNA in 20-µl final volume, using M-MuLV reverse transcriptase and oligo-dT (18 mer) primer (Fermentas GmbH, Germany). PCR amplifications were performed using PCR mixture (15 µl) that contained 1 µl of RT reaction product as template, 1x PCR buffer, 200-µM dNTPs (Fermentas GmbH), 1 U of Taq DNA polymerase (New England Biolabs, Ipswitch, MA). The gene-specific primers for the genes AtPGP1, AtATH1 and AtATH10 were designed using Primer3 software (Table 1) and synthesized (IDT, USA). PCR was performed at initial denaturation at 94°C for 4 min, 30 or 22 cycles (1 min at 94°C; 0.5 min at 55 or 60°C; 0.5 min at 94°C), and final elongation (10 min at 72°C) using a thermal cycler (Biorad, Hercules, CA). The PCR products obtained were separated on 1.4% agarose gel, stained with ethidium bromide (0.001%), and documented in a gel documentation system (Innotech, USA). The size of the amplification product was estimated from the 100-bp DNA ladder (Fermentas GmbH). The band intensity of each gel was checked using the Herolab E.A.S.Y Win 32 software (Herolab GmbH Laborgerate). The transcript levels of each gene in kin plants were taken for comparison in calculating the transcript abundance of respective genes.

Table 1.

Gene-specific primers and annealing temperatures used for RT-PCR

Primer Sequence (5′-3′) Annealing temperature (°C) Gene bank ID Fragment size (bp)
AtPGP1 Forward TTG TGG GTC CAA GCG GGT GC 60 At2g36910 249
AtPGP1 Reverse GCA CTG GCT AGA GTC GCG GC
AtATH1 Forward GCT CTT GTG GGT CCA AGC GGG 55 At2g36910 215
AtATH1 Reverse TGC GCA CTG GCT AGA GTC GC
AtATH10 Forward GAC GCT CAT GTC CAA GCC GG 62 At4g01660 189
AtATH10 Reverse GGG ACG GTG GCT CCA AGC TT
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Experimental design and data analysis.

Each experiment was conducted on two occasions with a total of at least 33 replications. All the observations and calculations were made separately for each set of experiments and were expressed as mean ± standard deviation. The data were subjected to one-way ANOVA and mean separations were performed by Duncan's multiple range test for segregating means where the level of significance was set at p ≤ 0.05.38

Acknowledgments

We thank Kristin Bubel and Rafael Castaneda for their help with measuring plants.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

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