Arbuscular Mycorrhizal Fungus Funneliformis Mosseae Research Articles

Editorial: Control of Plant Pathogens by Biogenic Elicitors and Possible Mechanisms of Action.

Editorial: Control of Plant Pathogens by Biogenic Elicitors and Possible Mechanisms of Action.

Gr and hp-1 tomato mutants unveil unprecedented interactions between arbuscular mycorrhizal symbiosis and fruit ripening.

Systemic responses to an arbuscular mycorrhizal fungus reveal opposite phenological patterns in two tomato ripening mutants depending whether ethylene or light reception is involved. The availability of tomato ripening mutants has revealed many aspects of the genetics behind fleshy fruit ripening, plant hormones and light signal reception. Since previous analyses revealed that arbuscular mycorrhizal symbiosis influences tomato berry ripening, we wanted to test the hypothesis that an interplay might occur between root symbiosis and fruit ripening. With this aim, we screened seven tomato mutants affected in the ripening process for their responsiveness to the arbuscular mycorrhizal fungus Funneliformis mosseae. Following their phenological responses we selected two mutants for a deeper analysis: Green ripe (Gr), deficient in fruit ethylene perception and high-pigment-1 (hp-1), displaying enhanced light signal perception throughout the plant. We investigated the putative interactions between ripening processes, mycorrhizal establishment and systemic effects using biochemical and gene expression tools. Our experiments showed that both mutants, notwithstanding a normal mycorrhizal phenotype at root level, exhibit altered arbuscule functionality. Furthermore, in contrast to wild type, mycorrhization did not lead to a higher phosphate concentration in berries of both mutants. These results suggest that the mutations considered interfere with arbuscular mycorrhiza inducing systemic changes in plant phenology and fruits metabolism. We hypothesize a cross talk mechanism between AM and ripening processes that involves genes related to ethylene and light signaling.

Effects of the Timing of Herbivory on Plant Defense Induction and Insect Performance in Ribwort Plantain (Plantago lanceolata L.) Depend on Plant Mycorrhizal Status.

Plants often are exposed to antagonistic and symbiotic organisms both aboveground and belowground. Interactions between above- and belowground organisms may occur either simultaneously or sequentially, and jointly can determine plant responses to future enemies. However, little is known about time-dependency of such aboveground-belowground interactions. We examined how the timing of a 24 h period of aboveground herbivory by Spodoptera exigua (1–8 d prior to later arriving conspecifics) influenced the response of Plantago lanceolata and the performance of later arriving conspecifics. We also examined whether these induced responses were modulated by the arbuscular mycorrhizal fungus (AMF) Funneliformis mosseae. The amount of leaf area consumed by later arriving herbivores decreased with time after induction by early herbivores. Mycorrhizal infection reduced the relative growth rate (RGR) of later arriving herbivores, associated with a reduction in efficiency of conversion of ingested food rather than a reduction in relative consumption rates. In non-mycorrhizal plants, leaf concentrations of the defense compound catalpol showed a linear two-fold increase during the eight days following early herbivory. By contrast, mycorrhizal plants already had elevated levels of leaf catalpol prior to their exposure to early herbivory and did not show any further increase following herbivory. These results indicate that AMF resulted in a systemic induction, rather than priming of these defenses. AMF infection significantly reduced shoot biomass of Plantago lanceolata. We conclude that plant responses to future herbivores are not only influenced by exposure to prior aboveground and belowground organisms, but also by when these prior organisms arrive and interact.

Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus.

Roots of most terrestrial plants form symbiotic associations (mycorrhiza) with soil- borne arbuscular mycorrhizal fungi (AMF). Many studies show that mycorrhizal colonization enhances plant resistance against pathogenic fungi. However, the mechanism of mycorrhiza-induced disease resistance remains equivocal. In this study, we found that mycorrhizal inoculation with AMF Funneliformis mosseae significantly alleviated tomato (Solanum lycopersicum Mill.) early blight disease caused by Alternaria solani Sorauer. AMF pre-inoculation led to significant increases in activities of β-1,3-glucanase, chitinase, phenylalanine ammonia-lyase (PAL) and lipoxygenase (LOX) in tomato leaves upon pathogen inoculation. Mycorrhizal inoculation alone did not influence the transcripts of most genes tested. However, pathogen attack on AMF-inoculated plants provoked strong defense responses of three genes encoding pathogenesis-related proteins, PR1, PR2, and PR3, as well as defense-related genes LOX, AOC, and PAL, in tomato leaves. The induction of defense responses in AMF pre-inoculated plants was much higher and more rapid than that in un-inoculated plants in present of pathogen infection. Three tomato genotypes: a Castlemart wild-type (WT) plant, a jasmonate (JA) biosynthesis mutant (spr2), and a prosystemin-overexpressing 35S::PS plant were used to examine the role of the JA signaling pathway in AMF-primed disease defense. Pathogen infection on mycorrhizal 35S::PS plants led to higher induction of defense-related genes and enzymes relative to WT plants. However, pathogen infection did not induce these genes and enzymes in mycorrhizal spr2 mutant plants. Bioassays showed that 35S::PS plants were more resistant and spr2 plants were more susceptible to early blight compared with WT plants. Our finding indicates that mycorrhizal colonization enhances tomato resistance to early blight by priming systemic defense response, and the JA signaling pathway is essential for mycorrhiza-primed disease resistance.

Arbuscular mycorrhiza affects nickel translocation and expression of ABC transporter and metallothionein genes in Festuca arundinacea

Mycorrhizal fungi are key microorganisms for enhancing phytoremediation of soils contaminated with heavy metals. In this study, the effects of the arbuscular mycorrhizal fungus (AMF) Funneliformis mosseae (=Glomus mosseae) on physiological and molecular mechanisms involved in the nickel (Ni) tolerance of tall fescue (Festuca arundinacea = Schedonorus arundinaceus) were investigated. Nickel addition had a pronounced negative effect on tall fescue growth and photosynthetic pigment contents, as well as on AMF colonization. Phosphorus content increased markedly in mycorrhizal plants (M) compared to non-inoculated (NM) ones. However, no significant difference was observed in root carbohydrate content between AMF-inoculated and non-inoculated plants. For both M and NM plants, Ni concentrations in shoots and roots increased according to the addition of the metal into soil, but inoculation with F. mosseae led to significantly lower Ni translocation from roots to the aboveground parts compared to non-inoculated plants. ABC transporter and metallothionein transcripts accumulated to considerably higher levels in tall fescue plants colonized by F. mosseae than in the corresponding non-mycorrhizal plants. These results highlight the importance of mycorrhizal colonization in alleviating Ni-induced stress by reducing Ni transport from roots to shoots of tall fescue plants.

The symbiosis between Nicotiana tabacum and the endomycorrhizal fungus Funneliformis mosseae increases the plant glutathione level and decreases leaf cadmium and root arsenic contents

Over time, anthropogenic activities have led to severe cadmium (Cd) and arsenic (As) pollution in several environments. Plants inhabiting metal(loid)-contaminated areas should be able to sequester and detoxify these toxic elements as soon as they enter roots and leaves. We postulated here that an important role in protecting plants from excessive metal(loid) accumulation and toxicity might be played by arbuscular mycorrhizal (AM) fungi. In fact, human exploitation of plant material derived from Cd- and As-polluted environments may lead to a noxious intake of these toxic elements; in particular, a possible source of Cd and As for humans is given by cigarette and cigar smoke. We investigated the role of AM fungus Funneliformis mosseae (T.H. Nicolson & Gerd.) C. Walker & A. Schüßler in protecting Nicotiana tabacum L. (cv. Petit Havana) from the above-mentioned metal(loid) stress. Our findings proved that the AM symbiosis is effective in increasing the plant tissue content of the antioxidant glutathione (GSH), in influencing the amount of metal(loid)-induced chelators as phytochelatins, and in reducing the Cd and As content in leaves and roots of adult tobacco plants. These results might also prove useful in improving the quality of commercial tobacco, thus reducing the risks to human health due to inhalation of toxic elements contained in smoking products.

Phosphate concentration and arbuscular mycorrhizal colonisation influence the growth, yield and expression of twelve PHT1 family phosphate transporters in foxtail millet (Setaria italica).

Phosphorus (P) is an essential element which plays several key roles in all living organisms. Setaria italica (foxtail millet) is a model species for panacoid grasses including several millet species widely grown in arid regions of Asia and Africa, and for the bioenergy crop switchgrass. The growth responses of S. italica to different levels of inorganic phosphate (Pi) and to colonisation with the arbuscular mycorrhizal fungus Funneliformis mosseae (syn. Glomus mosseae) were studied. Phosphate is taken up from the environment by the PHT1 family of plant phosphate transporters, which have been well characterized in several plant species. Bioinformatic analysis identified 12 members of the PHT1 gene family (SiPHT1;1-1;12) in S. italica, and RT and qPCR analysis showed that most of these transporters displayed specific expression patterns with respect to tissue, phosphate status and arbuscular mycorrhizal colonisation. SiPHT1;2 was found to be expressed in all tissues and in all growth conditions tested. In contrast, expression of SiPHT1;4 was induced in roots after 15 days growth in hydroponic medium of low Pi concentration. Expression of SiPHT1;8 and SiPHT1;9 in roots was selectively induced by colonisation with F. mosseae. SiPHT1;3 and SiPHT1;4 were found to be predominantly expressed in leaf and root tissues respectively. Several other transporters were expressed in shoots and leaves during growth in low Pi concentrations. This study will form the basis for the further characterization of these transporters, with the long term goal of improving the phosphate use efficiency of foxtail millet.

Arbuscular mycorrhiza mediates glomalin-related soil protein production and soil enzyme activities in the rhizosphere of trifoliate orange grown under different P levels.

Glomalin-related soil protein (GRSP) is beneficial to soil and plants and is affected by various factors. To address whether mycorrhizal-induced GRSP and relevant soil enzymes depend on external P levels, a pot study evaluated effects of the arbuscular mycorrhizal fungus (AMF) Funneliformis mosseae on GRSP production and soil enzyme activities. Three GRSP categories, as easily-extractable GRSP (EE-GRSP), difficultly-extractable GRSP (DE-GRSP), and total (EE-GRSP + DE-GRSP) GRSP (T-GRSP), were analyzed, together with five enzyme activities (β-glucosidase, catalase, peroxidase, phosphatase, polyphenol oxidase) in the rhizosphere of trifoliate orange (Poncirus trifoliata) grown under 0, 3, and 30mM KH2PO4 in a sand substrate. After 4months, root AM colonization and substrate hyphal length decreased with increasing P levels. Shoot, root, and total biomass production was significantly increased by AM colonization, regardless of P levels, but more profound under 0mM P than under 30mM KH2PO4. In general, production of these three GRSP categories under 0 or 30mM KH2PO4 was similar in non-mycorrhizosphere but decreased in mycorrhizosphere. Mycorrhization significantly increased the production of EE-GRSP, DE-GRSP and T-GRSP, soil organic carbon (SOC), and activity of substrate β-glucosidase, catalase, peroxidase, and phosphatase, but decreased polyphenol oxidase activity, irrespective of P levels. Production of EE-GRSP, DE-GRSP, and T-GRSP significantly positively correlated with SOC and β-glucosidase, catalase, and peroxidase activity, negatively with polyphenol oxidase activity, but not with hyphal length or phosphatase activity. These results indicate that AM-mediated production of GRSP and relevant soil enzyme activities may not depend on external P concentrations.

Arbuscular mycorrhizal fungi alleviate oxidative stress induced by ADOR and enhance antioxidant responses of tomato plants

The behaviour of tomato plants inoculated with arbuscular mycorrhizal (AM) fungi grown in the presence of aqueous extracts from dry olive residue (ADOR) was studied in order to understand how this symbiotic relationship helps plants to cope with oxidative stress caused by ADOR. The influence of AM symbiosis on plant growth and other physiological parameters was also studied. Tomato plants were inoculated with the AM fungus Funneliformis mosseae and were grown in the presence of ADOR bioremediated and non-bioremediated by Coriolopsis floccosa and Penicillium chrysogenum-10. The antioxidant response as well as parameters of oxidative damage were examined in roots and leaves. The data showed a significant increase in the biomass of AM plant growth in the presence of ADOR, regardless of whether it was bioremediated. The establishment and development of the symbiosis were negatively affected after plants were exposed to ADOR. No differences were observed in the relative water content (RWC) or PS II efficiency between non-AM and AM plants. The increase in the enzymatic activities of superoxide dismutase (SOD; EC 1.15.1.1), catalase (CAT; EC 1.11.1.6) and glutathione-S-transferase (GST; EC 2.5.1.18) were simultaneous to the reduction of MDA levels and H2O2 content in AM root growth in the presence of ADOR. Similar H2O2 levels were observed among non-AM and AM plants, although only AM plants showed reduced lipid peroxidation content, probably due to the involvement of antioxidant enzymes. The results highlight how the application of both bioremediated ADOR and AM fungi can alleviate the oxidative stress conditions, improving the growth and development of tomato plants.

Comparison of systemic and local interactions between the arbuscular mycorrhizal fungus Funneliformis mosseae and the root pathogen Aphanomyces euteiches in Medicago truncatula

It has been shown in a number of pathosystems that arbuscular mycorrhizal (AM) fungi confer resistance against root pathogens, including in interactions between Medicago truncatula and the root rot-causing oomycete Aphanomyces euteiches. For the current study of these interactions, a split root system was established for plant marker gene analysis in order to study systemic defense responses and to compare them with local interactions in conventional pot cultures. It turned out, however, that split root systems and pot cultures were in different physiological stages. Genes for pathogenesis-related proteins and for enzymes involved in flavonoid biosynthesis were generally more highly expressed in split root systems, accompanied by changes in RNA accumulation for genes encoding enzymes involved in phytohormone biosynthesis. Against expectations, the pathogen showed increased activity in these split root systems when the AM fungus Funneliformis mosseae was present separately in the distal part of the roots. Gene expression analysis revealed that this is associated in the pathogen-infected compartment with a systemic down-regulation of a gene coding for isochorismate synthase (ICS), a key enzyme of salicylic acid biosynthesis. At the same time, transcripts of genes encoding pathogenesis-related proteins and for enzymes involved in the biosynthesis of flavonoids accumulated to lower levels. In conventional pot cultures showing decreased A. euteiches activity in the presence of the AM fungus, the ICS gene was down regulated only if both the AM fungus and the pathogen were present in the root system. Such negative priming of salicylic acid biosynthesis could result in increased activities of jasmonate-regulated defense responses and could explain mycorrhiza-induced resistance. Altogether, this study shows that the split root system does not reflect a systemic interaction between F. mosseae and A. euteiches in M. truncatula and indicates the importance of testing such systems prior to the analysis of mycorrhiza-induced resistance.

Enhancing ecosystem services in sustainable agriculture: Biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi

Arbuscular mycorrhizal fungi (AMF) establishing beneficial symbiosis with most crop plants have gained a growing interest as agro-ecosystem service providers able to sustain crop productivity and quality. In this study we tested the agronomic relevance of field-inoculated locally sourced and foreign inocula on chickpea (Cicer arietinum L.), one of the most important worldwide grain legumes. The foreign AMF Funneliformis mosseae and Rhizophagus irregularis were used as single and dual species inocula. Crop growth and productivity, plant nutrient uptakes and protein, Fe and Zn grain biofortification were assessed under a rainfed low-input cropping system after autumn and spring sowings. Uni- and multivariate analyses of data showed that AM fungal field inoculation increased chickpea AM fungal root colonization as well as plant biomass and yield. In addition, AMF were also effective in improving the nutritional value of grain by protein, Fe and Zn biofortification. The locally sourced AM fungal inoculum was more efficient then the foreign ones in Fe and Zn grain biofortification and, in the spring sowing treatment, also in improving yield and grain protein content. These findings enhance our understanding of the field potential role of AMF showing that a mycorrhiza-friendly approach in agriculture may have great potential in biofertilization of crops and biofortification of foods.

Impact of Arbuscular Mycorrhizal Fungi with Trichoderma viride and Pseudomonas fluorescens on Growth Enhancement of Genetically Modified Bt Cotton (Bacillus thuringiensis)

The present investigation was undertaken to find out efficient strains of Arbuscular mycorrhizal (AM) fungi (Funneliformis mosseae and Acaulospora laevis) alone or in combinations with Pseudomonas fluorescens and Trichoderma viride on growth parameters of Bt cotton (Bacillus thuringiensis) var. NCS-108 (SUNNY). All inoculated seedlings showed significant biomass production than control seedlings. Triple inoculation of A. laevis + T. viride + P. fluorescens showed maximum increment in plant height, fresh and dry root weight, root length, total chlorophyll content, shoot phosphorus content, root phosphorus content, both acidic, and alkaline phosphatase activity, whereas fresh and dry shoot weight, leaf area, AM spore number, and stomatal conductance were found maximum in the combination F. mosseae + A. laevis + T. viride. Maximum fiber yield was found in the combination of F. mosseae + A. laevis + T. viride + P. fluorescens. These results indicate that triple inoculation of A. laevis + T. viride + P. fluorescens followed by the combination F. mosseae + A. laevis + T. viride showed significant response for inoculating Bt cotton in order to get significant growth and field with maximum yield.

The arbuscular mycorrhizal symbiosis attenuates symptom severity and reduces virus concentration in tomato infected by Tomato yellow leaf curl Sardinia virus (TYLCSV)

The arbuscular mycorrhizal (AM) symbiosis is considered a natural instrument to improve plant health and productivity since mycorrhizal plants often show higher tolerance to abiotic and biotic stresses. However, the impact of the AM symbiosis on infection by viral pathogens is still largely uncertain and little explored. In the present study, tomato plants were grown under controlled conditions and inoculated with the AM fungus Funneliformis mosseae. Once the mycorrhizal colonization had developed, plants were inoculated with the Tomato yellow leaf curl Sardinia virus (TYLCSV), a geminivirus causing one of the most serious viral diseases of tomatoes in Mediterranean areas. Biological conditions consisted of control plants (C), TYLCSV-infected plants (V), mycorrhizal plants (M), and TYLCSV-infected mycorrhizal plants (MV). At the time of analysis, the level of mycorrhiza development and the expression profiles of mycorrhiza-responsive selected genes were not significantly modified by virus infection, thus indicating that the AM symbiosis was unaffected by the presence and spread of the virus. Viral symptoms were milder, and both shoot and root concentrations of viral DNA were lower in MV plants than in V plants. Overall F. mosseae colonization appears to exert a beneficial effect on tomato plants in attenuating the disease caused by TYLCSV.

Arbuscular mycorrhizal fungi and Trichoderma viride mediated Fusarium wilt control in tomato

The biocontrol potential of two arbuscular mycorrhizal fungi (AMF) (Funneliformis mosseae and Acaulospora laevis) and Trichoderma viride was assessed against tomato wilt caused by Fusarium oxysporum Schlecht. f. sp. lycopersici under pot condition. All the bioagent showed appreciable results in increasing plant growth. Combined inoculation of F. mosseae, A. laevis and T. viride showed maximum increases in plant height, shoot fresh weight, root dry weight, number of leaves and number of branches per plant while dual inoculation of F. mosseae and T. viride increased rest of the growth parameters like shoot dry weight, root fresh weight, root length and leaf area. AM colonisation and spore number was found highest in single inoculation of AMF, which decreases with the addition of T. viride. But, this decrease has no effect on biocontrol efficiency of bioagents. Photosynthesis, chlorophyll content and nutrient content were markedly decreased by pathogen infection. Bioagent application overcomes this effect and a remarkable increase in the plant phosphorus and nitrogen content was recorded. Among both the AMF, F. mosseae proved to be more effective strain compared to A. laevis for tomato. Maximum reduction in disease incidence and severity was recorded in combined inoculation of F. mosseae, A. laevis and T. viride. Whereas control plants without any bioagent showed maximum occurrence of disease. The findings of this study concludes that soil inoculation with F. mosseae along with root inoculation with conidial suspension of T. viride before transplantation offered better survival and resistance to tomato seedlings against Fusarium wilt.

Functional characterisation and transcript analysis of an alkaline phosphatase from the arbuscular mycorrhizal fungus Funneliformis mosseae

Alkaline phosphatases (ALP) in arbuscular mycorrhizal (AM) fungi have been suggested to be involved in transfer of phosphate from the mycorrhizal fungus to the host plant, but exact mechanisms are still unknown, partially due to the lack of molecular information. We isolated a full-length cDNA (FmALP) from the AM fungus Funneliformis mosseae (syn. Glomus mosseae) showing similarity with putative ALP genes from Rhizophagus intraradices (syn. Glomus intraradices) and Gigaspora margarita. For functional characterisation FmALP was expressed heterologously in the yeast Pichia pastoris. The recombinant FmALP protein had a pH optimum of 9.5, and catalysed the hydrolysis of glycerolphosphate and, to a lesser extent of glucose-1- and 6-phosphate, confirming it to be an alkaline phosphatase belonging to the family of alkaline phosphomonoesterases (EC 3.1.3.1). FmALP did not catalyse the hydrolysis of ATP or polyP. Relative FmALP transcript levels were analysed in intra- and extraradical hyphae isolated from F. mosseae infected ryegrass (Lolium perenne) using reverse transcription-quantitative polymerase chain reaction (RT-qPCR). FmALP was highly expressed in intraradical hyphae at low Pi supply, and its expression was repressed by high Pi supply. Taken together this study provides evidence for mycorrhizal alkaline phosphatases playing a role in P mobilisation from organic substrates under P starvation conditions.

Multifaceted potential of bioinoculants on red bell pepper (F1 hybrid, Indam Mamatha) production

The present investigation was undertaken to determine the comparative efficacy of two arbuscular mycorrhizal (AM) fungi (Funneliformis mosseae and Acaulospora laevis) with Trichoderma viride and Pseudomonas fluorescens on growth and yield of red bell pepper. The results indicate that F. mosseae colonized the plant roots better as compared to A. laevis and promoted maximum increment in AM spore number, root colonization, leaf area, acid phosphatase activity, early fruit formation along with maximum increase in fruit nitrogen, and protein content. Whereas F. mosseae+P. fluorescens promoted maximum increase in plant height, shoot weight, mycorrhizal dependency, chlorophyll a, alkaline phosphatase activity, and fruit phosphorus content. Regarding root length, root weight, leaf photosynthesis, chlorophyll b, number of fruits per plant and their fresh weight, it was found best in F. mosseae+A. laevis+P. fluorescens. Therefore, soil inoculation with suitable bioinoculant should be used at nursery stage for better yield.