The Role of Tomato and Corn Root Exudates on Glomus mosseae Spores Germination and Ralstonia solanacearum Growth in vitro
An in vitro experiment was conducted to study the effect of different plant root exudates on germination of Glomus mosseae and the growth of bacterial wilt Ralstonia solanacearum. Mycorrhizal spore germination increased when the volume of Mycorrhizal Tomato Root Exudates (MTRE) increased and in contrast, a negative relationship was recorded when the volume of Non-Mycorrhizal Tomato Root Exudates (NMTRE) increased. Similarly, the Mycorrhizal Corn Root Exudates (MCRE) was able to increase the percentage of germinated spores as compared to the Non-Mycorrhizal Corn Root Exudates (NMCRE). The antagonistic effect between Ralstonia solanacearum and Glomus mosseae was also studied in this research. There was no inhibition effect of mycorrhizal and non-mycorrhizal tomato and corn root exudates on growth of R. solanacearum. The study indicated that Glomus mosseae spore germination could be influenced by the host plant or pH medium.
Plant root exudates play a key role during the presymbiotic growth phase and
have been shown to stimulate hyphal branching and the catabolic metabolism of
Arbuscular Mycorrhizal (AM) fungal spores (Bücking
et al., 2008). Exudates components are thought to attract beneficial
micro-organisms to the rhizosphere and also to promote their survival in this
particular environment (Bayliss et al., 1997).
Many scientific studies have been carried out using in vitro systems
and new prospects have been opened up by using the material provided by monoxenic
plates (Cano et al., 2008). Plant root exudates
consist mainly on a complex mixture of organic acid anions, phytosiderophores,
purines, sugar, vitamins, amino acids, nucleosides, inorganic ions (e.g., HCO3¯,
OH¯, H+), gaseous molecules (CO2, H2),
enzymes and root border cells (Dakora and Phillips, 2002).
The first in vitro culture of AMF under aseptic conditions was accomplished
by Mosse (1962). The life cycle of AMF is initiated
by germination of spores (Smith and Read, 1997). The using
of transformed-root organ cultures in vitro showed that volatile substances
from roots were active (function) in the early stages of VAM formation (Linderman,
1994). Many factors can affect spore germination of AMF such as root exudates
and/or volatiles, soil moisture, pH, light, temperature and CO2 (Giovannetti,
The sporulation of the oomycete Phytophthora fragriae was reduced after
using root exudates from a strawberry plant in in vitro studies (Norman
and Hooker, 2000). It is well documented that changes in specific chemical
components in plant tissues could deter pathogens. The germination of soil-borne
fungus Fusarium oxysporum f. sp. lycopersici was inhibited in
the presence of root exudates of tomato plants (Scheffknecht
et al., 2006).
Treatment of tomato root exudates with insoluble polyvinylpolypyrrolidone,
which binds phenolic compounds, indicated that tomato root exudates contain
phenolic compounds inhibitory to Fusarium oxysporum f. sp. lycopersici
microconidia germination. On the opposite, in the same study, non polyvinylpolypyrrolidone
treated tomato root exudates stimulate microconidia germination of both F.
oxysporum f. sp. lycopersicy and F. oxysporum f. sp. radicis-lycopersici
(Steinkellner, 2005). It is well established that in
vitro AM production is an appropriate way of getting large amounts of clean,
clonal, contamination-free AM fungal material. This has opened new research
opportunities for molecular biology and biochemical techniques to be applied
to mycorrhizal research and the direct consequence of this is an exponential
increase in our knowledge in the basic biology of this mutualistic symbiosis
over the last 10 years (Cano et al., 2008).
The using of mycorrhizal fungi as biocontrol agents against soil-borne pathogens
under the field conditions is well documented (Smith and Read,
2008). Arbuscular mycorrhizal fungi have shown a direct interaction with
soil-borne pathogen through antagonism, mycoparasitism and/or antibiosis (Harrier
and Watson, 2004). Ralstonia solanacearum is a soil-borne pathogen
that causes bacterial wilt diseases in diverse plant species (Yao
and Allen, 2007).
Split root experiments revealed that R. solanacearum was inhibited by
the mycorrhizal fungus Glomus versiforme as a result of increased phenols
content induced systemically but to a lesser extent than locally (Zhu
and Yao, 2004).
Root exudates could be use for the multiplication of mycorrhizal fungi another spores in vitro because it serve as signals that initiate the symbiosis mechanisms of mycorrhizal fungi and the in vitro control ability of root exudates on the phytopathogenic bacteria R. solanacearum could be the first step in the management of bacterial wilt disease based on exudates compounds.
The current study consists of two experiments; the first experiment was aimed to evaluate the ability of different root exudates germination of G. mosseae spores. The second experiment was aimed to study the interaction between the mycorrhizal fungi G. mosseae germinated spores and R. solanacearum under laboratory controlled conditions.
MATERIALS AND METHODS
Experiment 1: Root Exudates Production
This study was done at the Laboratory of Soil Microbiology, Land Management
Department, Universiti Putra Malaysia, Malaysia. Four types of root exudates
||Mycorrhizal Tomato Root Exudates (MTRE) colonized by G.
||Non-Mycorrhizal Tomato Root Exudates (NMTRE)
||Mycorrhizal Corn Root Exudates Colonized (MCRE) with G. mosseae
||Non-Mycorrhizal Corn Root Exudates (NMCRE)
Root exudates from colonized plants were produced following the method described
by Shang et al. (2000). Seeds of red rock tomato
cultivar and corn plants were rinsed for 15-20 sec with 95% ethanol for surface
disinfestation. The seeds were washed several times with sterilized and distilled
water. The seeds (five seeds/flask) from both plant species were placed separately
in sterile glass flasks (50 mL), containing 10 mL of sterile deionized water.
The flasks were covered with cotton and sterile aluminum foil and were kept
in growth chamber at 28°C in the dark for seed germination. The flasks were
open after 14 days under laminar-flow and the solution of root exudates was
collected using sterile Pasteur pipette. The exudates solution was immediately
passed through 0.45 μm filter to remove root debris; the solution was stored
at 4°C for 1 week before use. It was checked for microbial contamination.
One milliliter from each exudates was taken three times and cultured on Potato
Dextrose Agar (PDA) media before quantification and incubated at 28°C for
5 days. Exudates from AMF non colonized tomato roots were produced using the
method described by Karlos and Safir (1987). Plants were
taken from the soil (30 days old), the roots were washed carefully with distilled
water and then rinsed with sterile distilled water several times. About 20-30
seedlings were placed in a flask containing 100 mL of sterile distilled water
for 24 h. The solution was concentrated 1/10 of the original volume by rotary
evaporation at 50°C, filtered again and stored at 4°C. The product was
checked for microbial contamination by plating 1 mL on PDA and incubated at
28°C for 5 days.
Amino Acids Analysis
Amino acid concentrations were determined using HPLC by a modified method
from Cohen (1994) following pre-column derivatisation
with AQC reagent (6-aminoquinolyl-N-hydroxysuccinimdyl carbamate, Waters, USA).
Tryptophan content was determined by alkaline hydrolyses. Cysteine and methionine
were not determined.
Glomus mosseae, Isolation and Collection
Mature spores of G. mosseae for the experiments were collected from
a stock culture (Land Management Department, Universiti Putra Malaysia). The
spores were transferred using a sterilized pipette to 0.45 μm diameter
filter paper disc. The system was autoclaved (121°C for 15 min) before spore
Water Agar (WA) (8%) was used as culture media. Ten milliliters of media
was dispensed into glass Petri dish (9 cm diameter). The media was mixed with
different volumes (2, 4, 6, 8, 10 and 12 mL) of the different root exudates
separately. The media was adjusted to pH 6.5 using potassium chloride (KCl).
The plates were kept in refrigerator at 4°C overnight before used.
Spore Surface Disinfestations
Before G. mosseae spores were cultured between both filter paper
discs, the 2% chloramines T, 400 mg of streptomycin and 1 drop of Tween 80%
L-1 distilled water was used for spore surface disinfestation. The
solution passed through a 0.22 μm membrane until the first drop of the
solution emerged. The contact time between solution and spores was 15-20 min.
The spores were washed 5 times with sterilized and distilled water before plating
onto Petri dishes. The spores were singly transferred to Petri dish (10 spores/dish)
Ten spores of Glomus mosseae numbers for each replicates were transferred
to sterilized filter paper (0.45 μm) by using sterilized forceps. The spores
were distributed in the filter paper and placed on 9 cm Petri-dish with WA.
Petri-dishes with spores were incubated in the dark at room temperature (28±2°C).
After 5 days of spore's culture in different substrate, the germ tube was clearly
observed for germinated spores after filter paper staining (Phillips
and Hayman, 1970). Germinated spores were counted under binocular microscope
at 100x; the color of germinated spores was yellow to brownish. The media was
adjusted for all exudates to pH 6.5 using KCl before any treatment and it was
measured after 5 days of spore culture. Data were analyzed by linear regression
analysis to determine the relationship between percentage of spore germination
and root exudate concentration using excel microsoft 2007.
Experiment 2: Root Exudates Production (As in Experiment 1) Bacterial
According to Nesmith and Jenkins (1979), bacterial
inoculums of R. solanacearum was prepared. Casamino acid Peptone Glucose
(CPG) agar media according to Cuppelss et al. (1978).
Inoculum was prepared by using bacterial suspension that was adjusted to 108
cfu mL-1 using a spectrophotometer at OD600 = 0.8. The
bacterial suspension was prepared from a 24 h old culture. Ten milliliters of
the suspension was inoculated into each test tube containing different volumes
of different root exudates. Test tubes were incubated in at 26±2°C
for 24 h.
Different volumes of different root exudates were mixed with a R. solanacearum
suspension (108 cfu mL-1) (5 mL/test tube). The mixture
was kept in incubator for 48 h at 26-28±2°C.
RESULTS AND DISCUSSION
Experiment 1: Root Exudates Quantification
Sixteen amino acids were analyzed for the four types of root exudates (Table
1). Four replicates from each exudate were tested. All root exudates were
analyzed by standard Analysis of Variance (ANOVA) and treatments means were
compared using the Tukeys comparison test at p<0.01 using the SPSS
software. ANOVA was performed for each amino acid detected.
|| Amino acid contents in different types of root exudates
|Mean values in rows followed by the same letter(s) are not
significantly different, according to Tukeys HSD (p<0.01), were
as, MTRE: Mycorrhizal tomato root exudates colonized by G. mosseae,
NMTRE: Non-mycorrhizal tomato root exudates, MCRE: Mycorrhizal corn root
exudates, NMCRE: Non-mycorrhizal corn root exudates. ANOVA was preformed
for each amino acid
|| Relationship between different volumes of Mycorrhizal Tomato
Root Exudates (MTRE) and Glomus mosseae spore germination after 5
days of in vitro culture of the mycorrhizal fungi
||Relationship between different volumes of Non-Mycorrhizal
Tomato Root Exudates (NMTRE) and Glomus mosseae spores germination
after 5 days of in vitro culture of mycorrhizal fungi
Spore Germination (%)
A negative linear relationship was observed between MTRE and percentage
spore germination (R2 = 0.97) (Fig. 1), i.e., spore
germination percentage decreased with increasing the volumes of mycorrhizal
tomato root exudates.
On the opposite the percentage of G. mosseae spore germination was increased linearly by increasing NMTRE volume (R2 = 0.92) (Fig. 2).
A negative linear relationship was observed between spore germination number and exudates volume (R2 = 0.91) (Fig. 3).
A positive linear relationship was recorded between NMCRE volume and the number of germinated spores (R2 = 0.94) (Fig. 4).
Experiment 2: Bacterial Concentration (cfu)
The concentration of R. solanacearum bacterial cell in a mixture
of the bacteria and serial volumes of different root exudates was measured.
Ralstonia solanacearum concentration decreased as mycorrhizal tomato
root exudates volume increased, as indicated by the negative linear relationship
observed between this two variables (R2 = 0.97) (Fig.
Negative relationship between NMTRE and R. solanacearum cell concentration was observed (R2 = 0.93) (Fig. 6).
MCRE was influenced on R. solanacearum growth negatively; the growth of R. solanacearum was not inhibited by increasing the MCRE volume (Fig. 7).
||Relationship between different volumes of Mycorrhizal Corn
Root Exudates (MCRE) and Glomus mosseae spores germination after
5 days of in vitro culture of mycorrhizal fungi
||Relationship between Non-Mycorrhizal Corn Root Exudates (NMCRE)
and Glomus mosseae spores germination after 5 days of in vitro
culture of mycorrhizal fungi
||Relationship between different volume of Mycorrhizal Tomato
Root Exudates (MTRE) and the cfu of the Ralstonia solanacearum spore
suspension after 48 h of incubation at 26-28± 2°C
A negative linear effect was observed between root exudates volumes of mycorrhizal corn and bacterial concentration (R2 = 0.93) (Fig. 8).
The pH changes in a mixture of R. solancearum cell suspension and
serial volumes of different root exudates was measured at the end of the experiment.
The pH of the bacterial suspension increased linearly with the MTRE volume increase
(R2 = 0.98) (Fig. 9).
||Relationship between different volumes of Non-Mycorrhizal
Tomato Root Exhudates (NMTRE) and the cfu of the Ralstonia solanacearum
cell suspension after 48 h of incubation at 26-28±2°C
||Relationship between different volumes of Mycorrhizal Corn
Root Exudates (MCRE) and cfu of the Ralstonia solanacearum cell suspension
after 48 h of incubation at 26-28±2°C
||Relationship between different volume of Non-Mycorrhizal Corn
Root Exudates (NMCRE) and cfu of the Ralastonia solanacearum cell
suspension after 48 h of incubation at 26-28 ±2°C
Similarly, a positive linear relationship was found (R2 = 0.98) between NMTRE volume and pH (Fig. 10).
The pH of the mixture R. solanacearum and root exudates was positive and linearly correlated with exudates of NMCRE increasing volumes (R2 = 0.90) (Fig. 11).
||Relationship between pH and volume of a Mycorrhizal Tomato
Root Exudates (MTRE) mixed with a Ralstonia solanacearum cell suspension
after 48 h of incubation at 26-28±2°C
||Relationship between pH and volume of a Non-Mycorrhizal Tomato
Root Exudates (NMTRE) mixed with a Ralstonia solanacaerum cell suspension
after 48 h of incubation at 26-28±2°Cbetween pH and volume of
a Non-Mycorrhizal Corn Root Exudates (NMCRE) mixed with a Ralstonia solanacearum
cell suspension after 48 h of incubation at 26-28±2°C
||Relationship between pH and volume of a Non-Mycorrhizal Corn
Root Exudates (NMCRE) mixed with a Ralstonia solanacearum cell suspension
after 48 h of incubation at 26-28±2°C
A positive relationship was also detected (R2 = 0.98) between the volume of MCRE and pH value of the suspension (Fig. 12).
The present study presents a method to evaluate the effect of different root
exudates in mycorrhizal fungi germination spores. Differences in spore germination
of AMF due to root exudation source and quality were reported among some types
of exudates, for example, root exudates of cucumber mycorrhized plants showed
a reduced stimulatory effect on AM hyphal growth and an inhibitory effect on
root colonization by AMF (Vierheilig and Piche, 2003).
||Relationship between pH and volume of Mycorrhizal Corn Root
Exudates (MCRE) mixed with a Ralstonia solanacearum cell suspension
after 48 h of incubation 26-28±2°C
Similarly, Norman and Hooker (2000) found that root
exudates from mycorrhized strawberry plants reduced the sporulation of Phytophthora
fragariae. Present findings disagree with the results reported by Douds
and Nagahashi (2000) as they found that the rate of spore germination can
be increased by plant host root exudates. In the same way, Büching
et al. (2008) found that crude exudation led to a slight acceleration
of spore germination and increased germ tube branching. Siu
and Donald (1991) stated that in vitro production of flavonoids from
alfalfa roots (Medicago sativa L.) may regulate or facilitate the development
of AMF symbioses and offer new hope for developing pure plant-free culture of
Root exudates components such as flavonoids and volatiles (CO2,
H2) produced due to the germination of mycorrhizal spores were the
main reasons behind the germination of AMF, but the sporulation rate was reduced
according to the amount of exudates used. The results obtained from this study
were in the same line with that reported by Chabot et
al. (1992), who suggested that hyphal growth of the Vesicular Arbuscular
Mycorrhizal (VAM) fungus, Gigaspora margarita Becker and Hall, is affected
by stimulatory flavonoids compounds (kaempferol, quercetin and morin).
Root exudates quantity was an important factor for spore germination number.
Present data agree with that reported by Schwab et al.
(1983), in which the quantity and composition of root extracts may not be
a reliable predictor of the availability of the substrate for symbiotic VAM
fungi. The data suggested that exudates quantity and quality were important
stimulatory factors for spore germination. These results contradict with those
obtained by Karlos and Safir (1987), they documented
that the quality of exudates only an important in stimulating VAM fungus germination
and hyphal elongation. The same results were confirmed by Vierheilig
and Piche (2003), they observed that root exudates of non-mycorrhizal cucumber
plants show a significant stimulatory effect on root colonization.
In present study, the spore germination was stimulated better by increasing
the volume of NTRE and NCRE. These results can be explained by the quality of
exudates used which contain more substances that stimulate the spore germination.
Current results agree with the data published by Lioussanne
et al. (2003) they suggested that root exudates collected from non-mycorrhizal
tomato roots exhibited a higher attracting effect on zoospore of Phytophthora
parasitica than root exudates from mycorrhizal tomato roots.
However, this results disagree with that published by Hepper
and Smith (1976), who found that the spores of Acaulospora lavis
maintained a few weeks at 6°C were exposed to different pH levels and germination
was higher in low pH. Another report was recorded by Bücking
et al. (2003) they found that root exudates supplied to AM fungal spores
in various concentrations significantly affect germination and hyphal branching
of AMF spores in in vitro. Ralstonia solanacearum growth was negatively
affected by using serial volumes of root exudates produced from corn and tomato
plants. The cell concentration of R. solanacearum decreased when the
volume of the root exudates (all types) increased. these results conflected
with those published by Scheffknecht et al. (2006)
they found that microconidia of F. oxysporum f. sp. lycopersici
was enhanced in the presence of root exudates from mycorrhizal plant.
Quantification of tomato and corn root exudates colonized by AMF indicated
that, amino acids were produced in a high quantity by the plant but the R.
solanacearum was not suppressed by using different volume of MTRE. The pathogen
strain (race 3 biovare 2) might explain the aggressive in vitro growth
The effect of root exudates from mycorrhizal and nonmycorrhizal tomato plants
on germination of the tomato pathogen F. oxysporum f sp. lycopersici
was tested by Scheffknecht et al. (2006). They
found that germination of F. oxysporum f. sp. lycopersici microconidia
was enhanced in the presence of mycorrhizal tomato root exudates. These results
were in the same line with the results that establish how R. solanacearum
growth increased by the different root exudates types used in the study.
The authors would like to acknowledge Universiti Putra Malaysia for funding this project (Grant No. 01-02-04-0394-EA001).
Bayliss, C., E. Bent, D.E. Culham, S. MacLellan, A.J. Clarke, G.L. Brown and J.M Wood, 1997.
Bacterial genetic loci implicated in the Pseudomonas putida
GR12-2R3-canola mutualism: Identification of an exudates-inducible sugar transporter. Can. J. Microbiol., 43: 809-818.PubMed | Direct Link |
Bucking, H., J. Abubaker, M. Govindarajulu, M. Tala and P.E. Pfeffer et al
Root exudates stimulate the uptake and metabolism of organic carbon in germinating spores of Glomus intraradices
. New Phytologist, 180: 684-695.CrossRef | PubMed | Direct Link |
Bucking, H., J. Abubaker, M. Govindarajulu, P.E. Pfeffer, P. Lammers and Y. Shachar-Hill, 2003.
The effect of root exudates on spore germination, uptake, metabolism and gene expression of the arbuscular mycorrhizal fungus Glomus intraradices
. Proceedings of the International Conference on Mycorrhiza, April 30, 2003, Microbial Biophysics and Residue Chemistry Research /USDA/USA., pp: 282-282Direct Link |
Cano, C., S. Dickson, M.G. Guerrero and A. Bago, 2008. In vitro
Cultures Open New Prospects for Basic Research in ARBUSCULAR MYCorrhizas. In: Mycorrhiza: in Mycorrhiza, State of the Art, Genetics and Molecular Biology, Eco-Function, Biotechnology, Eco-Physiology, Structure and Systematics, Varma, A. (Ed.). 3rd Edn., Springer, Germany, ISBN: 978-3-540-78824-9, pp: 627-654
Chabot, S., R. Bel-Rhlid, R. Chenevert and Y. Piche, 1992.
Hyphal growth promotion in vitro
of the VA mycorrhizal fungus, Gigaspora margarita
Becker and Hall, by the activity of structurally specific flavonoid compounds under CO2
enriched conditions. New Phytol., 122: 461-467.CrossRef | Direct Link |
Cohen, S.A., 2003.
Amino acid analysis using pre-column N
-derivatization with 6-aminoquinolyl-hydroxysuccinimidyl carbamate. Methods Mol. Biol., 211: 143-154.CrossRef | Direct Link |
Cuppels, D.A., R.S. Hanson and A. Kelman, 1978.
Isolation and characterization of a bacteriocin produced by Pseudomonas solanacearum
. J. Gen. Microbiol., 109: 295-303.Direct Link |
Dakora, F.D. and D.A. Phillips, 2002.
Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil, 245: 35-47.CrossRef | Direct Link |
Douds, D.D. and G. Nagahashi, 2000.
Signalling and Recognition Events Prior to Colonisation of Roots by Arbuscular Mycorrhizal Fungi. In: Current Advances in Mycorrhizae Research, Podila, G. and D.D. Douds (Eds.). APS Press, Minnesota, ISBN: 0-89054-245-7, pp: 11-18Direct Link |
Karlos, S.E. and G.R Safir, 1987.
Hyphal elongation of Glomus fasciculatus
in response to root exudates. Applied Environ. Microbiol., 53: 1928-1933.Direct Link |
Giovannetti, M., 2000.
Spore germination and Pre-Symbiotic Mycelia Growth. In: Arbuscular mycorrhizas
: Physiology and Function, Kapulink, Y. and D.D. David (Eds.). 1st Edn., Springer, Germany, ISBN-10: 0792364449, pp: 47-68Direct Link |
Harrier, L.A. and C.A. Watson, 2004.
The potential role of Arbuscular Mycorrhizal (AM) fungi in the bioprotection of plants against soil-borne pathogens in organic and/or other sustainable farming systems. Pest Manage. Sci., 60: 149-157.CrossRef | Direct Link |
Hayward, A.C., 1991.
Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum
. Annu. Rev. Phytopathol., 29: 65-87.CrossRef | Direct Link |
Hepper, C.M. and G.A. Smith, 1976.
Observations on the germination of Endogone
spores. Trans. Br. Mycol. Soc., 66: 189-194.Direct Link |
Linderman, R.G., 1994.
Role of VAM Fungi in Biocontrol. In: Mycorrhizae and Plant Health, Pfleger, F.L. and R.G. Linderman (Eds.). The American Phytopathological Society, St. Paul, MN., USA., ISBN: 0-89054-158-2, pp: 1-27Direct Link |
Lioussanne, L., M. Jolicoeur and M. St-Arnaud, 2003.
Effects of alteration of tomato root exudation by Glomus intraradices
colonization on Phytophthora parasitica
var. nicotianae zoospores. Proceedings of the 4th International Conference on Mycorrhizae (ICOM4), August 10-15, 2003, Montereal, Que, pp: 291-291
MacDonald, R.M., 1981.
Routine production of axenic vesicular-arbuscular mycorrhizal. New Phytol., 89: 87-93.CrossRef | Direct Link |
Mosse, B., 1962.
The establishment of vesicular-arbuscular mycorrhiza under aseptic conditions. J. Gen. Microbiol., 27: 509-520.CrossRef | Direct Link |
Nesmith, W.C. and S.F. Jenkins, 1979.
A selective medium for the isolation and quantification, of Pseudomonas solanacearum
from soil. Phytopathology, 67: 182-185.Direct Link |
Norman, J.R. and J.E. Hooker, 2000.
Sporulation of Phytophthora fragaria
shows greater stimulation by exudates of non-mycorrhizal than by mycorrhizal strawberry roots. Mycol. Res., 104: 1069-1073.Direct Link |
Phillips, J. and D.S. Hayman, 1970.
Improved procedure for clearing roots and staining parasitic and vesicular mycorrizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc., 55: 185-185.
Scheffknecht, S., R. Mammerler, S. Steinkellner and H. Vierheilig, 2006.
Root exudates of mycorrhizal tomato plants exhibit a different effect on microconidia germination of Fusarium oxysporum
f. sp. lycopersici
than root exudates from non-mycorrhizal tomato plants. Mycorrhiza, 16: 365-370.CrossRef | Direct Link |
Schwab, S.M., J.A. Menge and T.L. Robert, 1983.
Quantitative and qualitative effects of phosphorus on extracts and exudates of sudangrass roots in relation to vesicular-arbuscular mycorrhiza formation. Plant Physiol., 73: 761-765.PubMed | Direct Link |
Shang, H., C.R. Grau and R.D. Peters, 2000.
Oospore.Germination of Aphanomyces euteiches in root exudates and on the rhizoplanes of crop plants. Plant Dis., 84: 994-998.CrossRef | Direct Link |
Tsai, S.M. and D.A. Phillips, 1991.
Flavonoids released naturally from alfalfa promote development of symbiotic Glomus
spores in vitro
. Applied Environ. Microbiol., 57: 1485-1488.PubMed | Direct Link |
Smith, S.E. and D.J. Read, 1997.
Mycorrhizal Symbiosis. 2nd Edn., Academic Press, London, ISBN: 0126528403 Direct Link |
Smith, S.E. and D.J. Read, 2008.
Mycorrhizal Symbiosis. 3rd Edn., Academic Press, London, UK., ISBN-13: 978-0123705266, Pages: 800Direct Link |
Steinkellner, S., R. Mammerler and H. Vierheilig, 2005.
Microconidia germination of the tomato pathogen Fusarium oxysporum
in the presence of root exudates. J. Plant Interact., 1: 23-30.CrossRef | Direct Link |
Yao, J. and C. Allen, 2007.
The plant pathogen Ralstonia solanacearum
needs aerotaxis for normal biofilm formation and interactions with its tomato host. J. Bacteriol., 189: 6415-6424.CrossRef | Direct Link |
Vierheilig, H., S. Lerat and Y. Piche, 2003.
inhibition of mycorrhiza development by root exudates of cucumber plants colonized by Glomus mosseae
. Mycorrhiza, 13: 167-170.CrossRef | Direct Link |
Zhu, H.H. and Q. Yao, 2004.
Localized and systemic increase of phenols in tomato roots induced by Glomus versiforme
inhibits Ralstonia solanacearum
. J. Phytopathol., 152: 537-542.CrossRef | Direct Link |