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. 2007 Jan-Feb;2(1):58–62. doi: 10.4161/psb.2.1.3884

Colonization by Arbuscular Mycorrhizal Fungi of Sorghum Leads to Reduced Germination and Subsequent Attachment and Emergence of Striga hermonthica

Venasius W Lendzemo 1, Thomas W Kuyper 2,✉, Radoslava Matusova 3, Harro J Bouwmeester 3, Aad Van Ast 4
PMCID: PMC2633899  PMID: 19516969

Abstract

Two sorghum cultivars: the Striga-tolerant S-35 and the Striga-sensitive CK60-B were grown with or without arbuscular mycorrhizal (AM) fungi, and with or without phosphorus addition. At 24 and 45 days after sowing (DAS) of sorghum, root exudates were collected and tested for effects on germination of preconditioned Striga hermonthica seeds. Root exudates from AM sorghum plants induced lower germination of S. hermonthica seeds than exudates from non-mycorrhizal sorghum. The magnitude of this effect depended on the cultivar and harvest time. A significantly (88–97%) lower germination of S. hermonthica seeds upon exposure to root exudates from AM S-35 plants was observed at both harvest times whereas for AM inoculated CK60-B plants a significantly (41%) lower germination was observed only at 45 DAS. The number of S. hermonthica seedlings attached to and emerged on both sorghum cultivars were also lower in mycorrhizal than in non-mycorrhizal plants. Again, this reduction was more pronounced with S-35 than with CK60-B plants. There was no effect of phosphorus addition on Striga seed germination, attachment or emergence. We hypothesize that the negative effect of mycorrhizal colonization on Striga germination and on subsequent attachment and emergence is mediated through the production of signaling molecules (strigolactones) for AM fungi and parasitic plants.

Key Words: arbuscular mycorrhiza, root exudate, sorghum, striga, strigolactones, germination

Introduction

Sorghum is one of the major food grain crops in the world, especially in developing countries. In savannah regions of Africa where sorghum is one of the major staple foods, it is particularly overwhelmed by infestation by the root hemiparasite Striga hermonthica (Del.) Benth. (Orobanchaceae). Efforts to combat Striga had very little effect to date. Reasons for the limited success in Striga control include prolific seed production, close coupling of its life cycle to that of its host, and the fact that effective control methods are not within the reach of farmers practicing subsistence agriculture.1

The symbiosis between sorghum roots and arbuscular mycorrhizal (AM) fungi influences the S. hermonthica-sorghum interaction. Colonization by AM fungi reduced attachment and emergence of S. hermonthica on sorghum.2–5 The underlying mechanisms for the lower performance of Striga on cereal crops upon AM fungal colonization are unknown. Preliminary investigations suggested that colonization by AM fungi also reduced seed germination of S. hermonthica.4 In order to germinate, Striga seeds require signal molecules that are exuded by the roots of their hosts, called germination stimulants. These signal molecules belong to the class of the strigolactones.6 Strigolactones have recently also been identified as signal molecules in the earliest stage of the interaction between plant roots and AM fungi.7–9 This double role for strigolactones suggests that the non-mycorrhizal Orobanchaceae have hijacked the molecular communication between host plants and AM fungi.

Vierheilig10 reviewed the regulatory mechanisms during the interaction between host plants and AM fungi. He noted that AM plants show autoregulation, i.e., plants that are colonized by an AM fungus suppress subsequent colonization by AM fungi through altered root exudation.11–12 Vierheilig10 proposed the hypothesis of “one mechanism-two symptoms”, i.e., the possibility that changed root exudates not only autoregulate further mycorrhizal colonization but also repress soil pathogens that are attracted to the root by the same compounds in the exudate. This hypothesis has not been investigated for Striga.

The objective of this study was therefore to investigate whether root exudates from mycorrhizal and non-mycorrhizal sorghum plants differ in their ability to induce germination of S. hermonthica seeds. To study this we used two cultivars of sorghum and reared them in the presence or absence of AM fungi and with or without phosphorus addition. We investigated the effect of these treatments on the induction of S. hermonthica seed germination, attachment and emergence.

Materials and Methods

Plant material and growth conditions.

The experiments were conducted at Wageningen University during July–August 2003 in a greenhouse with simulated tropical conditions. Daylength was regulated at 12 h using black screens. The average temperature in the greenhouse varied between 25–36°C during the day and 23–35°C at night. Relative humidity varied between 53–68% during the day and 68–71% at night. Sorghum was grown in a mixture of 1:3 of arable soil and coarse sand. This soil/sand mixture was gamma-radiated at 10 kGy. The arable soil had a pH-KCl of 6.7, organic matter content of 1.3% and total N content of 0.05%. Plants were grown in 2-litre black plastic pots filled with 2 kg of the sterilized soil/sand mixture, with drainage holes in the bottom. The design was a full factorial with three factors: AM fungal inoculum (absent and 50 g per pot), P (0 and 30 kg P ha−1 as triple superphosphate) and S. hermonthica [0 and 5 mg (≈1000 germinable seeds) per pot]. The eight treatments were applied in five replicates to two sorghum cultivars, the Striga-tolerant S-35 and the Striga-sensitive CK60-B in a randomized complete block design. Plants were harvested at 24 and 45 days after sowing (DAS).

The AM fungal soil inoculum was a mixture of propagules of Glomus clarum Nicolson and Schenck and Gigaspora margarita Becker and Hall.2 The S. hermonthica seeds were harvested from plants growing on sorghum in Mali in 1998. The seeds for each pot were mixed with quartz sand (50 g) in aluminum trays and kept moist for 10 days in the greenhouse to precondition. A similar amount of quartz sand without S. hermonthica seeds was treated similarly. The sand/S. hermonthica seeds mix, inoculum of AM fungi, P fertilizer or their combinations were mixed with the top 6 cm soil in the pots in the relevant treatments. The control treatments were established at the same time: moist quartz sand was mixed with soil in the upper 6 cm of the pots that did not receive Striga seeds, whereas 50 g of gamma-radiated soil inoculum of AM fungi was mixed through the soil in pots that did not receive inoculum of AM fungi. A microbial wash13 was used in all treatments by suspending 50 g mycorrhizal inoculum in 500 ml water and passing the solution through a filter. Three pregerminated sorghum seeds were planted in each pot and thinned to one per pot just after emergence. Plants were watered with tap water throughout the experiment. No fertilizer was applied apart from triple superphosphate at the start of the experiment. Striga emergence and the number of shoots were recorded daily. At each harvest, the soil was carefully washed off the roots and the numbers of attached Striga recorded.

Sorghum plants from the treatments without Striga were placed in glass beakers with sufficient (70 ml for the first and 250 ml for the second harvest) demineralized water to keep the whole root system immersed. The roots were kept in darkness by wrapping aluminum foil around the beakers. After 36 h the solution in the beakers was collected and used in a Striga germination bioassay.

Germination bioassay.

Striga seeds were surface sterilized in 2% sodium hypochlorite containing 0.02% (v/v) Tween 20 for 5 minutes, subsequently rinsed with sterile demineralized water, and dried for 30 minutes in a laminar air flow cabinet. For preconditioning, 80–100 surface sterilized Striga seeds were placed on moistened (with 50 µl of sterile demineralized water) glass microfibre filter paper (GMFP) discs (1 cm diam.), placed in sterile Petri dishes lined with one layer of Whatman filter paper (90 mm diam.). To keep the seeds moist during preconditioning, the filter paper was wetted with 3 ml of sterile demineralized water. The Petri dishes were sealed with parafilm, wrapped in aluminum foil and subsequently kept in an incubator at 30°C for 21 days to ascertain optimal sensitivity to germination stimulants.14 After preconditioning, the GMFP discs containing Striga seeds were dried for 20 minutes in a laminar air flow cabinet and 5 GMFP discs placed in the middle of each Petri dish lined with a ring (1.0 cm wide) of filter paper. The filter paper ring was moistened with 0.9 ml sterile demineralized water. To each cluster of seeds on a GMFP disc, 50 µl root exudate was applied. As positive control, 50 µl of GR24 (0.1 mg l−1), a synthetic germination stimulant (provided by the Department of Organic Chemistry, Radboud University, Nijmegen, The Netherlands), was used to ascertain germinability of seeds. Sterile demineralized water served as negative control. All Petri dishes were sealed with parafilm, wrapped in aluminum foil and incubated at 30°C for five days. Germinated and non-germinated seeds were counted under a dissecting microscope (× 50 magnification). Seeds were considered germinated when germ tubes were clearly visible.

Fractional root colonization and biomass determination.

After root exudates were collected, approximately 2 g (fresh weight) of roots were cut and chopped into roughly 1-cm fragments, stained in 0.01% Trypan blue in lacto-glycerol and evaluated for mycorrhizal colonization with the gridline-intersect method. Subsequently, root and shoot fresh weight were determined and the plant material dried at 80°C for 24 h in an oven to determine dry matter content.

Data analysis.

Because we could not exclude the possibility that germination of Striga seeds stimulates neighboring seeds in vitro, we used the non-parametric Mann-Whitney U test for fractional germination. In one treatment with the cultivar S-35, no Striga emerged. Because these data did not meet the requirements for ANOVA, the Kruskal-Wallis test was used to test for significance of effects of mycorrhiza and phosphorus on number of attached or emerged Striga. Data on sorghum biomass were subjected to ANOVA using the statistical package SAS® System for Windows (8th edition).

Results

Sorghum root colonization by AM fungi.

In the non-mycorrhizal treatments, sorghum roots remained free of AM fungal colonization. Colonization levels at 24 DAS varied between 3 and 5% and at 45 DAS between 27 and 44%. Colonization levels were similar between the treatments irrespective of cultivar differences or P addition.

Germination of preconditioned S. hermonthica seeds on exposure to root exudates.

No Striga seeds germinated on exposure to sterile demineralized water. Root exudates collected from non-mycorrhizal sorghum plants induced germination of Striga seeds. Germination was higher at the second than at the first harvest. At first harvest (24 DAS) Striga germination varied between 6 and 13%, whereas 45 DAS Striga germination varied between 41 and 52%, only slightly lower than germination induced by GR 24 (62%). There was no significant effect of P fertilization on Striga germination. Root exudates from AM sorghum plants induced lower Striga germination (Table 1).

Table 1.

Percentage germination of S. hermonthica seeds after exposure to GR24 (0.1 mg l−1) or to sorghum root exudates

S-35 CK60-B
Treatment Harvest 1 Harvest 2 Harvest 1 Harvest 2
GR24 52.6 61.7 52.6 61.7
—AM—P 13.3 48.5 6.2 41.1
—AM+P 12.3 49.8 5.7 52.3
+AM—P 1.6 2.5 1.3 29.1
+AM+P 1.4 0.9 4.0 26.4
Mann-Whitney U-test
Mycorrhiza ** ** n.s. **
Phosphorus n.s. n.s. n.s. n.s.
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Root exudates were obtained from two sorghum cultivars (S-35, CK60-B) grown for 24 (harvest 1) or 45 (harvest 2) days with AM fungal inoculation (−AM = no inoculation; +AM = addition of 50 g per pot) and/or P (−P = no addition of P fertilizer; +P = addition of the equivalence of 30 kg ha-1 of triple superphosphate). Values are means of five replicates. Mann-Whitney U-test: n.s. not significant (P > 0.05);

**

P < 0.01.

The magnitude of the mycorrhizal effect was cultivar-dependent. The reduction in germination by mycorrhizal root exudates of S-35 was significant at both harvests whereas the effect of mycorrhizal root exudates of CK60-B was only significant at the second harvest. With root exudates from mycorrhizal S-35 plants, germination of Striga seeds was 3–12% (second and first harvest respectively) of that of non-mycorrhizal plants. In contrast, germination of Striga seeds after exposure to root exudates from mycorrhizal CK60-B plants was 45–59% (first and second harvest respectively) of that of non-mycorrhizal plants (Table 1).

Attached and emerged Striga.

In none of the treatments Striga seedlings were observed on sorghum roots at 24 DAS. At 45 DAS significantly higher numbers of Striga had attached and emerged in the non-mycorrhizal treatments. In the AM treatments, both the numbers of attached, but still below ground, and emerged Striga were significantly lower. This reduction in numbers was much larger for S-35 than for CK60-B. Almost no (94% reduction) Striga were attached to the root systems of treatments of S-35 that received AM fungal inoculum compared to 53% reduction in CK60-B. Number of Striga emerged showed the same trend. There was no P effect on the number of attached and emerged Striga (Table 2).

Table 2.

Effect of AM fungal inoculation and P addition on the number of Striga attached or emerged on two sorghum cultivars (S-35, CK60-B) at 45 DAS

S-35 CK60-B
Attached Emerged Attached Emerged
—AM—P 8.2a 2.8a 18.6a 11.2a
—AM+P 7.6a 3a 16.6a 6.6a
+AM—P 0.4b 0b 8.8b 5.4b
+AM+P 0.6b 0.2b 7.8b 6.2b
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For explanation of parameters see (Table 1). Values are means of five replicates. In each column means followed by the same letter are not significantly different (Kruskal-Wallis test, P < 0.05).

Sorghum performance.

At the first harvest there were no significant effects of Striga, AM fungal inoculation or P addition on sorghum biomass. By 45 DAS mycorrhizal plants of both cultivars had a significantly lower biomass than non-mycorrhizal plants. Striga reduced above-ground sorghum biomass in CK60-B but had no effect on root biomass. In S-35 Striga caused a small decrease in stem biomass but a large increase in root biomass. P application increased biomass in CK60-B, especially of roots, and had no effect on S-35 (data not shown).

Discussion

Mycorrhizal mediation of Striga seed germination.

Germination of Striga seeds, which is induced by root exudates, was significantly lower with exudates of AM sorghum plants. As far as we are aware, this suppression due to AM colonization has not been demonstrated before. We have now also confirmed suppression of Striga seed germination by AM maize (Bouwmeester HJ et al., unpublished).

The lower germination with root exudates of AM-sorghum can be explained in three ways. (i) The formation of metabolites that are responsible for the induction of Striga germination is Downregulated upon mycorrhizal colonization; (ii) (Plant) metabolites that are up-regulated upon mycorrhizal colonization inhibit Striga germination; (iii) Mycorrhizal colonization induces mycorrhizosphere effects that negatively impact on Striga germination.

Ad (i). downregulated compounds.

Strigolactones are the prime candidate for an explanation for reduced Striga seed germination upon mycorrhizal colonization. Strigolactones act as chemical signals for host plant recognition by AM fungi and as germination stimulants for Striga and Orobanche species.7–9 Root exudates (most likely strigolactones) induce a chemotropic reaction in Glomus mosseae, up to 1 mm from the root,15 comparable to the few mm over which the strigolactones act as germination stimulants. We envisage a mechanism whereby a host plant exudes strigolactones to attract AM fungi, but upon colonization reduces strigolactone exudation, resulting in autoregulation of mycorrhization and in lower Striga germination.

Ad (ii) upregulated compounds.

Levels of cyclohexenones, which arise through carotenoid degradation, were positively correlated with root colonization by AM-fungi.16 Germination stimulants of the Orobanchaceae are also derived from carotenoids.17 Fester et al.18 suggested that cyclohexenone levels accumulate with the concomitant degradation of arbuscules. However, Vierheilig et al19 reported that cyclohexenones are not accumulating systemically. Because mycorrhizal autoregulation is systemic10 and because we hypothesize that mycorrhizal autoregulation and reduced Striga seed germination is caused by the same underlying mechanism, we consider upregulation of cyclohexenone levels as explanation for reduced Striga germination unlikely. We are currently investigating whether mycorrhizal suppression of Striga seed germination is also systemic.

Ad (iii). Mycorrhizosphere effects.

Experiments with AM and non-mycorrhizal plants as a standard should involve a microbial wash.13 Through this microbial wash differences in bacterial composition between treatments and control should be eliminated. However, their use in experiments involving root exudates is not without difficulties. Certain bacteria live in close association with or are attached to AM fungi.20–21 Members of the bacterial genus Paenibacillus, described from the mycorrhizosphere of sorghum, stimulate mycorrhization and simultaneously show antagonistic activities against fungal pathogens and Phytophthora.22–23 Strains of Paenibacillus validus exude compounds that enhance hyphal branching after spore germination of Glomus intraradices.24–25

While our experiments do not, therefore, strictly show that the AM fungus is the sole causal agent for reduced germination of S. hermonthica seeds, we argue, in the light of the double role of strigolactones, that the mycorrhizal explanation is most parsimonious. Possible ways to test our proposed mechanism (mycorrhizal fungi autoregulate subsequent mycorrhization and simultaneously downregulate Striga germination through reduced production of strigolactones) is through the use of leaf materials, because strigolactones are produced in roots and shoots of sorghum9 and most likely maize.26 In such systems effects on the rhizosphere community could be eliminated. Alternatively, AM fungi can be grown under monoxenic conditions. In such a system other (micro-)organisms should be largely ruled out, although the contamination and increased secondary metabolite production on transformed roots could still be problematical.27

Effects of mycorrhizal colonization on Striga attachment and emergence.

Mycorrhizal sorghum plants also showed a significantly lower attachment and emergence of Striga. These results are consistent with earlier reports.2–5 While it is likely that this effect is explained through mycorrhizal effects on Striga germination, we cannot exclude further roles for AM fungi in affecting the performance of Striga. Mycorrhizal colonization can increase levels of cell wall-bound phenolics28 and induce expression of defense-related genes.29 Both mechanisms provide direct protection against antagonists. Improved nutrient status as a consequence of mycorrhizal colonization can also result in enhanced protection against pathogens.30

Effects of sorghum cultivar and phosphorus.

There were no differences in AM fungal colonization between both sorghum cultivars, even though mycorrhizal colonization of S-35 reduced Striga seed germination more than that of CK60-B. Gworgwor and Weber,3 however, noted that Glomus mosseae, which colonized sorghum plants to a higher degree than other AM fungi, also had a stronger suppressive effect on Striga emergence.

The lower Striga germination with exudates of AM colonized sorghum was not due to an improved P status of sorghum. There were no effects of P on number of germinating, attaching and emerging Striga, both in the mycorrhizal and non-mycorrhizal condition. No growth response of sorghum to P was observed either, indicating that plants were most likely not P-limited. Vierheilig10 reviewed the effect of P status of the plant on fungal responses to plant signals. Root exudates of P-fertilized plants result in a reduced stimulation of spore germination and hyphal growth. Recently, Yoneyama and coworkers31 showed that P-deficient red clover seedlings strongly promoted the exudation of the strigolactone orobanchol. Mechanisms how P availability affects root exudate composition and how this relates to both mycorrhizal colonization and Striga seed germination are currently under investigation in our laboratories.

Implications for Striga management.

Changes in root exudate composition after colonization by AM fungi are an important factor in the tripartite interaction between sorghum, Striga and AM fungi. It could potentially also contribute to Striga-control, if mycorrhiza-affected changes in exudate (strigolactone) production in the field occur rapidly enough. Hart and Reader32 studied colonization strategies of 21 AM fungal isolates. Four species of Glomus and one species of Acaulospora colonized Allium porrum within one week. Root colonization of sorghum was observed seven days after addition of inoculum (Lendzemo VW, unpublished). We are currently investigating the rate at which strigolactone production responds to mycorrhizal colonization.

Finally, an important caveat may also be necessary. Because strigolactones are required by AM-fungi for rapid colonization of their hosts, selection of crop cultivars for lower induction of Striga germination may be traded off against selection for reduced mycorrhizal colonization. Considering the prevailing agro-ecological circumstances this could be detrimental as the important staple foods in sub-Saharan Africa are both dependent on and responsive to AM fungi. Rather, we suggest that agronomic research efforts should be directed towards improving rapid colonization by AM fungi, immediately after germination of the crop seed, and a rapid response of the host to this colonization by reducing strigolactone exudation. This may involve a larger reliance on the mycorrhizal network than on spore inoculum.

Acknowledgements

These investigations were supported by the Netherlands Foundation for the Advancement of Tropical Research (WOTRO) (to V.W.L.). HJB and RM also acknowledge funding by the Netherlands Organization for Scientific Research (NWO), the European Commission (INCO-DEV, ICA4-CT-2000-30012) and the Dutch Ministry of Agriculture, Nature Management and Fisheries (North-South Programme). We are grateful to L. Narvaez for help in executing the experiments and C.H. de Vos for discussions on root exudate analysis.

Footnotes

Previously published online as a Plant Signaling & Behavior E-publication: http://www.landesbioscience.com/journals/psb/abstract.php?id=3884

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