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Benefits Conferred on Plants
Abstract
It has long been known that under suboptimal conditions mycorrhized plants fare better than their non-mycorrhized counterparts. This applies to desert truffles as well: when conditions are less than favorable, plants that enter into mycorrhizal associations with desert truffles exhibit higher levels of transpiration, stomatal conductance, and photosynthesis. Furthermore, studies of the gene expression of a fungal aquaporin in the mycorrhizal state revealed negative correlations with plant physiological parameters, suggesting that there is some form of communication between the symbionts. In particular, fine-tuning of plant aquaporin gene expression is responsive to water availability. Consistent with results reported for other mycorrhizal fungi, mineral acquisition was higher in plants mycorrhized by desert truffles, as was photosynthesis. Girdling led to noticeable reduction in carbon assimilation in non-mycorrhized plants but only to a slight reduction in mycorrhized ones. In addition, not only was general chlorophyll content higher in plants forming associations with desert truffles, but the ratio of chlorophyll b to chlorophyll a was higher too, leading to improved light harvesting under the lower irradiance conditions typical of mornings and afternoons. Correspondingly, the calculated activation energy for onset of photosynthesis was lower for desert truffle-mycorrhized plants.
... It is considered that desert truffles are a source of medicinal substances with anti-inflammatory, immunosuppressive, antimutagenic, anticarcinogenic, antioxidant, and antiradical properties (19). The juice of the truffle (Terfezia claveryi) was used to treat trachoma patients, showing great promise for treatment methods in contrast with currently available synthetic antibiotics (20). ...
This study aimed to investigate the phytochemicals and cytotoxic properties of aqueous extracts of desert truffle, Terfezia boudieri Chatin and its host plant Helianthemum aegyptiacum (L.) Mill. The chemical composition of truffle is relatively higher than its host plants. Carbohydrate content showed the highest rate, but crude lipid showed the lowest rate in truffle and the host plant. Potassium is the highest concentration macro-element, and iron is the highest concentration of micro-element in the truffle and host plant. Compared to the several extracts tested, ethyl acetate extracts of the desert truffle, T. boudieri and host plant H. aegyptiacum (L.) Mill. gave the highest cytotoxic activity against five tested cancer cell lines (the human eye carcinoma cell line MP38, the human central nervous system cell line SF-268, the colorectal carcinoma cell line HCT116, the prostate cancer cell line DU-145 and the breast cancer cell line MDA). The active substances of truffles are more effective than the active substances of host plants in terms of cell mortality rate and nuclear condensation of cancer cells. Human eye cancer cells MP38 treated with truffle ethyl acetate extract showed a greater cell mortality rate than those treated with host plant ethyl acetate extract. Thus, it could be concluded that desert truffles have distinctive metabolites with powerful biological activities, such as antiproliferative activities, compared to the host plant's corresponding metabolites.
... These desert truffles are fungi that form mycorrhizal symbiosis with different plant species and this symbiosis is really what adapts to the drought in the areas where they live. This drought adaptation has been well characterized and studied and is based mainly on strategies to improve plant nutrition and photosynthesis (Kagan-Zur et al. 2014a;Morte et al. 2000;Turgeman et al. 2011), the water use efficiency (Morte et al. 2010), mycorrhizal root colonization (Navarro-Ródenas et al. 2012a, expression of fungal and plant aquaporins (Navarro-Ródenas et al. 2012b and catalase genes . ...
Desert truffles are hypogeous edible fungi that have been exclusively harvested in wild areas for hundreds of years. Land-use changes coupled with shifts in precipitation pattern and volume, as a result of climate change, have led to a decline in wild production of these fungi. Due to their high nutritional value, as well as rising market prices, efforts were stepped toward domestication more than 20 years ago. The present chapter describes the achievements made to understand the biology and diversity of these desert truffles which have helped to make this resource more sustainable. Most efforts to domesticate this natural resource have begun primarily with Terfezia claveryi Chatin. Biotechnological processes for mycorrhizal plant production as well as plantation management practices are analyzed with the experience accumulated to date. Terfezia cultivation is a totally organic crop, with minimum water irrigation, without the consumption of fertilizers or phytosanitary products and using native fungal and plant species. Thus, the longstanding tradition of desert truffle harvesting looks to the future, by adapting its domestication to modern agriculture.
... The first plantation of the desert truffle Terfezia claveryi was established in 1999 in south-east Spain (Murcia) (Honrubia et al. 2001), since when most of the data related to the biotechnological aspects of the production of mycorrhizal plants and plantation management practices have been compiled in three publications of Springer (Morte et al. 2008. More recently, additional information on desert truffles related to soil properties (Bonifacio and Morte 2014), the types of mycorrhiza (Roth-Bejerano et al. 2014), cryptic and new species (Bordallo and Rodriguez 2014), the benefits conferred on plants (Kagan-Zur et al. 2014a), ascocarp enzymes (Pérez-Gilabert et al. 2014), and cultivation Honrubia et al. 2014) have been published by our group in the first international and monographic book devoted to desert truffles by the same publisher (Kagan-Zur et al. 2014b). However, the increasing demand for this crop, in Spain and in other countries, has prompted a search for new strategies to increase ascocarp production in the field, to improve the production protocol of mycorrhizal plants, and to advance our knowledge of the biology and biodiversity of these desert truffles. ...
This chapter summarizes the latest basic and applied advances in desert truffle research carried out to improve our knowledge of the biodiversity, physiology, biotechnology, and cultivation of these hypogeous and edible fungi. ITS-rDNA sequences in phylo-geographic studies and host plant and soil pH characteristics have been the key to describing eight new desert truffle species. The production of desert truffle mycorrhizal plants has been improved by using β-cyclodextrin and bioreactors for mycelium culture and native beneficial bacteria (PGPR and MHB) to increase seedling survival and mycorrhization. Some fungal enzymes have also been characterized in Terfezia claveryi ascocarps. The presence of alkaline phosphatase both in mycelia and ascocarps indicates that this enzyme plays an important role during the life cycle of T. claveryi, while acid phosphatase might be involved in a process that takes place during the ascocarp stage. Numerous desert truffle plantations have been established in Spain in the last 10 years. A high density of mycorrhizal plants combined with a proper irrigation are two important factors to stimulate ascocarp production. The combination of a high rate of intracellular colonization together with the fine-tuned expression of fungal and plant aquaporins could result in a morpho-physiological adaptation of this symbiosis in drought conditions. Moreover, desert truffle sylviculture is proposed for improving truffle production and for conserving the natural areas where desert truffle grow.
... Ectomycrrhizal (ECM) and ectendomycorrhizal associations are mutualistic symbioses between plants and fungi that colonize the extracellular space in the host roots (Smith and Read 2008). The association has important beneficial effects on plant mineral nutrition, water acquisition, photosynthesis, and tolerance to abiotic and biotic stresses (Morte et al. 2000;Kagan-Zur et al. 2014). T. boudieri is characterized by its ability to form ectomycorrhizal lifestyle with the host plant but, under certain conditions, it can also form the less common endomycorrhizal lifestyle (Zaretsky et al. 2006ab). ...
The ectendomycorrhizal fungus Terfezia boudieri is known to secrete auxin. While some of the effects of fungal auxin on the plant root system have been described, a comprehensive understanding is still lacking. A dual culture system to study pre mycorrhizal signal exchange revealed previously unrecognized root-fungus interaction mediated by the fungal auxin. The secreted fungal auxin induced negative taproot gravitropism, attenuated taproot growth rate, and inhibited initial host development. Auxin also induced expression of Arabidopsis carriers AUX1 and PIN1, both of which are involved in the gravitropic response. Exogenous application of auxin led to a root phenotype, which fully mimicked that induced by ectomycorrhizal fungi. Co-cultivation of Arabidopsis auxin receptor mutants tir1-1, tir1-1 afb2-3, tir1-1 afb1-3 afb2-3, and tir1-1 afb2-3 afb3-4 with Terfezia confirmed that auxin induces the observed root phenotype. The finding that auxin both induces taproot deviation from the gravity axis and coordinates growth rate is new. We propose a model in which the fungal auxin induces horizontal root development, as well as the coordination of growth rates between partners, along with the known auxin effect on lateral root induction that increases the availability of accessible sites for colonization at the soil plane of fungal spore abundance. Thus, the newly observed responses described here of the root to Terfezia contribute to a successful encounter between symbionts.
In semi-arid soils, limited water and nitrogen (N) restrict biological activity and plant growth. As aridity increases, understanding mycorrhizae’s role in supporting plant communities and mitigating desertification is critical, especially that of common mycelial networks (CMN) linking an individual fungus with roots of multiple plants of the same or different species, impacting establishment, succession, and resilience. Although CMN research has been extensive in temperate forests and grasslands, its importance in semi-arid environments is still uncertain. This study aimed to determine whether CMN shared by semi-arid-adapted plants can assist in redistributing N from nutrient-rich sites to poor ones. We hypothesize CMN are an essential mechanism responding to spatial soil nutrient heterogeneity in semi-arid areas, aiding plant establishment and survival.
Complementary controlled experiments were conducted using compartmentalized mesocosms where only mycelia could mobilize nutrients, examining CMN 15N redistribution and whether plant age/size affects directionality. We used Helianthemum almeriense as the host plant forming an ectendomycorrhiza with the mycorrhizal fungus Terfezia claveryi. Experiments revealed 15N translocation to sink compartments at varying levels, with higher translocation where plants were present. Moreover, 15N contribution to plant N pools was significantly higher in 1-month-old seedlings versus adult plants. Under controlled conditions, hyphae appear as an effective conduit for N redistribution. The results provide initial evidence that CMN may help to redistribute N between rich and poor sites in semi-arid regions. Furthermore, the CMN may contribute to the survival of new mycorrhizal seedlings developing in desert truffle plantations or wild areas. This, in turn, advances knowledge on maintaining these ecosystems over time.
This study aims to investigate the effects of inoculation using Terfezia boudieri Chatin ascospores (ectomycorrhizal fungus) on growth, root colonization and nutrient status of Helianthemum sessiliflorum Desf. seedlings grown in pots on two-soil types (gypseous and sandy loam).
Mycorrhizal seedlings had significantly increased their height and leaf number compared to non mycorrhizal
ones. Regardless of mycorrhizal inoculation treatments, the plants growing on gypseous soil showed higher growth as compared to sandy loam one. It appears that inoculation with T. boudieri changed root morphology, increasing branching of first-order lateral roots of H. sessiliflorum seedlings. The highest root mycorrhizal colonization was recorded in inoculated seedlings on sandy loam soil (89%) when compared to gypseous one (52%). N, P and K concentrations in mycorrhizal seedlings were significantly improved by fungal inoculation. It can be concluded that inoculation of H. sessiliflorum with T. boudieri increased growth attributes and improved plant nutritional status
We have performed the isolation, functional characterization and expression analysis of aquaporins in roots and leaves of Helianthemum almeriense, in order to evaluate their roles in tolerance to water deficit. Five cDNAs, named HaPIP1;1, HaPIP1;2, HaPIP2;1, HaPIP2;2 and HaTIP1;1, were isolated from H. almeriense. A phylogenetic analysis of deduced proteins confirmed that they belong to the water channel proteins family. The HaPIP1;1, HaPIP2;1 and HaTIP1;1 genes encode functional water channel proteins, as indicated by expression assays in Saccharomyces cerevisiae, showing divergent roles in the transport of water, CO2 and NH3. The expression patterns of the genes isolated from H. almeriense, and of a previously described gene from Terfezia claveryi (TcAQP1), were analyzed in mycorrhizal and non-mycorrhizal plants cultivated under well-watered or drought stress conditions. Some of the studied aquaporins were subjected to fine-tuned expression only under drought stress conditions. A beneficial effect on plant physiological parameters was observed in mycorrhizal plants with respect to non-mycorrhizal ones. Moreover, stress induced a change in the mycorrhizal type formed, which was more intracellular under drought stress. The combination of a high intracellular colonization, together with the fine-tuned expression of AQPs, could result in a morpho-physiological adaptation of this symbiosis to drought conditions.
This study aims to investigate the effects of inoculation using Terfezia boudieri Chatin ascospores (ectomycorrhizal fungus) on growth, root colonization and nutrient status of Helianthemum sessiliflorum Desf. seedlings grown in pots on two-soil types (gypseous and sandy loam). Mycorrhizal seedlings had significantly increased their height and leaf number compared to non-mycorrhizal ones. Regardless of mycorrhizal inoculation treatments, the plants growing on gypseous soil showed higher growth as compared to sandy loam one. It appears that inoculation with T. boudieri changed root morphology, increasing branching of first-order lateral roots of H. sessiliflorum seedlings. The highest root mycorrhizal colonization was recorded in inoculated seedlings on sandy loam soil (89%) when compared to gypseous one (52%). N, P and K concentrations in mycorrhizal seedlings were significantly improved by fungal inoculation. It can be concluded that inoculation of H. sessiliflorum with T. boudieri increased growth attributes and improved plant nutritional status.
Physiological parameters of mycorrhizal symbiosis by Helianthemum almeriense and Terfezia claveryi in orchards were characterized under water deficit conditions. Our orchard included 40 mycorrhizal and 40 nonmycorrhizal
plants. Only mycorrhizal plants survived at the beginning of the experimental period, indicating dependency on fungal symbionts
in roots for survival. Drought stress significantly affected the mycorrhizal colonization percentage which was 70% in nonirrigated
mycorrhizal and 48% in irrigated mycorrhizal plants. No significant differences in plant growth were observed between nonirrigated
and irrigated mycorrhizal plants before and after drought stress. Stomatal conductance was more sensitive to water stress
than shoot water potential. It decreased more than two-fold under drought-stress compared to control mycorrhizal plants under
irrigation/light saturating conditions, indicating important stomatal closure with water deficit. Plants’ water use efficiency
improved with drought with stomatal conductance values below 0.3mol m−2 s−1. The ability to maintain open stomata and photosynthesis under drought increased carbon supply for growth, and ascocarp fruiting
which requires current photosynthates. Basically, H. almeriense shows a conservative water use strategy based mainly on avoiding drought stress by reducing stomatal conductance as soil
water potential decreases and atmospheric conditions dry. The results show that mycorrhizal H. almeriense plants maintain good physiological parameters with low soil matric potentials, thus making them an alternative agricultural
crop in arid/semi-arid areas.
KeywordsDesert truffle cultivation-Drought stress avoidance-Ectendomycorrhiza
Symbioses between plants and beneficial soil microorganisms like arbuscular-mycorrhizal fungi (AMF) are known to promote plant growth and help plants to cope with biotic and abiotic stresses. Profound physiological changes take place in the host plant upon root colonization by AMF affecting the interactions with a wide range of organisms below- and above-ground. Protective effects of the symbiosis against pathogens, pests, and parasitic plants have been described for many plant species, including agriculturally important crop varieties. Besides mechanisms such as improved plant nutrition and competition, experimental evidence supports a major role of plant defenses in the observed protection. During mycorrhiza establishment, modulation of plant defense responses occurs thus achieving a functional symbiosis. As a consequence of this modulation, a mild, but effective activation of the plant immune responses seems to occur, not only locally but also systemically. This activation leads to a primed state of the plant that allows a more efficient activation of defense mechanisms in response to attack by potential enemies. Here, we give an overview of the impact on interactions between mycorrhizal plants and pathogens, herbivores, and parasitic plants, and we summarize the current knowledge of the underlying mechanisms. We focus on the priming of jasmonate-regulated plant defense mechanisms that play a central role in the induction of resistance by arbuscular mycorrhizas.
Biotrophic interfaces are formed in mutualistic and parasitic plant–fungus interactions. They result from coordinated developmental programs in both partners and represent specialized platforms for the exchange of information and nutritional metabolites. New data on the establishment and the components of functional interfaces have been obtained in a number of ways. First, by isolation of symbiotically defective mutants; second, by characterization of new genes and their products; and, third, by the identification and localization of components of biotrophic interfaces, such as cell-wall proteins, H+-ATPases and nutrient transporters.
The influence of inorganic and organic phosphorus (P) and the absence of P in the culture medium on the type of mycorrhizal colonization formed (ecto-, ectendo-, or endomycorrhiza) during Helianthemum almeriense x Terfezia claveryi symbiosis in in vitro conditions was analyzed. This is the first time that the relative proportions of the different mycorrhizal types in mycorrhizal roots of H. almeriense have been quantified and statistically analyzed. The relative proportions of the mycorrhizal types depended on the P source in the medium, suggesting that it is the organic P form that induces the formation of intracellular colonization. The above association should be considered as a continuum between intra- and intercellular colonizations, the most appropriate term for defining it being ectendomycorrhiza. The influence of the endogenous concentration of P on plant growth was also analyzed. P translocation was observed from shoot to roots, especially in mycorrhizal plants because mycorrhizal roots showed higher growth than non-mycorrhizal roots and/or because of an extra P demand from mycelium inside the roots. Soluble and cell wall acid phosphatases activities from H. almeriense roots were kinetically characterized at optimum pH (5.0), using p-nitrophenyl phosphate as substrate, with K
m values of 3.4 and 1.8 mM, respectively. Moreover, the plant acid phosphatase and fungal alkaline phosphatases activities were histochemically localised in mycorrhizal H. almeriense roots by fluorescence with enzyme-labelled fluorescence substrate.
The movement of water through mycorrhizal fungal tissues and between the fungus and roots is little understood. It has been demonstrated that arbuscular mycorrhizal (AM) symbiosis regulates root hydraulic properties, including root hydraulic conductivity. However, it is not clear whether this effect is due to a regulation of root aquaporins (cell-to-cell pathway) or to enhanced apoplastic water flow. Here we measured the relative contributions of the apoplastic versus the cell-to-cell pathway for water movement in roots of AM and non-AM plants.
We used a combination of two experiments using the apoplastic tracer dye light green SF yellowish and sodium azide as an inhibitor of aquaporin activity. Plant water and physiological status, root hydraulic conductivity and apoplastic water flow were measured.
Roots of AM plants enhanced significantly relative apoplastic water flow as compared with non-AM plants and this increase was evident under both well-watered and drought stress conditions. The presence of the AM fungus in the roots of the host plants was able to modulate the switching between apoplastic and cell-to-cell water transport pathways.
The ability of AM plants to switch between water transport pathways could allow a higher flexibility in the response of these plants to water shortage according to the demand from the shoot.
Plants of Helianthemum almeriense were micropropagated on MS medium and inoculated in vitro with Terfezia claveryi mycelium on MH medium and vermiculite. Mycorrhizal (M) and non-mycorrhizal (NM) plants were subjected to a drought stress period of 3 weeks in greenhouse conditions with the soil matric potential maintained at –0.5 MPa. Drought stress did not affect the amount of mycorrhizal colonization. The survival rate of M plants at the end of the drought stress period was higher than that of NM plants. The water potential was higher in M plants than in NM plants by 14% in well-watered and 26% in drought stressed plants. Transpiration, stomatal conductance and net photosynthesis were higher in M plants than in NM plants. Transpiration was 92% higher in M plants than in NM plants under drought-stress conditions and 40% when irrigated. Stomatal conductance was 45% and 14% higher and net photosynthesis 88% and 54% higher, respectively, in M than in NM plants. Drought stressed M plants accumulated more N, P and K than drought-stressed NM plants. Reduced negative effects of drought stress on H. almeriense by the desert truffle T. claveryi could be ascribed to specific physiological and nutritional mechanisms, suggesting that this mycorrhizal symbiosis aids adaptation to arid climates.
Terfezia claveryi is a hypogeous mycorrhizal fungus belonging to the so-called "desert truffles," with a good record as an edible fungus and of considerable economic importance. T. claveryi improves the tolerance to water stress of the host plant Helianthemum almeriense, for which, in field conditions, symbiosis with T. claveryi is valuable for its survival. We have characterized cDNAs from T. claveryi and identified a sequence related to the aquaporin gene family. The full-length sequence was obtained by rapid amplification of cDNA ends and was named TcAQP1. This aquaporin gene encoded a functional water-channel protein, as demonstrated by heterologous expression assays in Saccharomyces cerevisiae. The mycorrhizal fungal aquaporin increased both water and CO(2) conductivity in the heterologous expression system. The expression patterns of the TcAQP1 gene in mycelium, under different water potentials, and in mycorrhizal plants are discussed. The high levels of water conductivity of TcAQP1 could be related to the adaptation of this mycorrhizal fungus to semiarid areas. The CO(2) permeability of TcAQP1 could be involved in the regulation of T. claveryi growth during presymbiotic phases, making it a good candidate to be considered a novel molecular signaling channel in mycorrhizal fungi.
The aim of this work was to evaluate the effects of selected mycorrhiza obtained in the urban environment on growth, leaf gas exchange, and drought tolerance of containerized plants growing in the nursery. Two-year-old uniform Acer campestre L., Tilia cordata Mill., and Quercus robur L. were inoculated with a mixture of infected roots and mycelium of selected arbuscular (maple, linden) and/or ectomycorrhiza (linden, oak) fungi and grown in well-watered or water shortage conditions. Plant biomass and leaf area were measured 1 and 2 years after inoculation. Leaf gas exchange, chlorophyll fluorescence, and water relations were measured during the first and second growing seasons after inoculation. Our data suggest that the mycelium-based inoculum used in this experiment was able to colonize the roots of the tree species growing in the nursery. Plant biomass was affected by water shortage, but not by inoculation. Leaf area was affected by water regime and, in oak and linden, by inoculation. Leaf gas exchange was affected by inoculation and water stress. V
cmax and J
max were increased by inoculation and decreased by water shortage in all species. F
v/F
m was also generally higher in inoculated plants than in control. Changes in PSII photochemistry and photosynthesis may be related to the capacity of inoculated plants to maintain less negative leaf water potential under drought conditions. The overall data suggest that inoculated plants were better able to maintain physiological activity during water stress in comparison to non-inoculated plants.
The host plant Helianthemum sessiliflorum was inoculated with the mycorrhizal desert truffle Terfezia boudieri Chatin, and the subsequent effects of the ectomycorrhizal relationship on host physiology were determined. Diurnal measurements revealed that mycorrhizal (M) plants had higher rates of photosynthesis (35%), transpiration (18%), and night respiration (49%) than non-mycorrhizal (NM) plants. Consequently, M plants exhibited higher biomass accumulation, higher shoot-to-root ratios, and improved water use efficiency compared to NM plants. Total chlorophyll content was higher in M plants, and the ratio between chlorophyll a to chlorophyll b was altered in M plants. The increase in chlorophyll b content was significantly higher than the increase in chlorophyll a content (2.58- and 1.52-fold, respectively) compared to control. Calculation of the photosynthetic activation energy indicated lower energy requirements for CO(2) assimilation in M plants than in NM plants (48.62 and 61.56 kJ mol(-1), respectively). Continuous measurements of CO(2) exchange and transpiration in M plants versus NM plants provided a complete picture of the daily physiological differences brought on by the ectomycorrhizal relationships. The enhanced competence of M plants to withstand the harsh environmental conditions of the desert is discussed in view of the mycorrhizal-derived alterations in host physiology.
Roots of most plants in nature are colonized by arbuscular mycorrhizal (AM) fungi. Among the beneficial effects of this symbiosis to the host plant is the transport of water by the AM mycelium from inaccessible soil water resources to host roots. Here, an aquaporin (water channel) gene from an AM fungus (Glomus intraradices), which was named GintAQP1, is reported for the first time. From experiments in different colonized host roots growing under several environmental conditions, it seems that GintAQP1 gene expression is regulated in a compensatory way regarding host root aquaporin expression. At the same time, from in vitro experiments, it was shown that a signaling communication between NaCl-treated mycelium and untreated mycelium took place in order to regulate gene expression of both GintAQP1 and host root aquaporins. This communication could be involved in the transport of water from osmotically favorable growing mycelium or host roots to salt-stressed tissues.
The efficiency of photosynthetic electron transport depends on the coordinated interaction of photosystem II (PSII) and photosystem I (PSI) in the electron-transport chain. Each photosystem contains distinct pigment-protein complexes that harvest light from different regions of the visible spectrum. The light energy is utilized in an endergonic electron-transport reaction at each photosystem. Recent evidence has shown a large variability in the PSII/PSI stoichiometry in plants grown under different environmental irradiance conditions. Results in this work are consistent with the notion of a dynamic, rather than static, thylakoid membrane in which the stoichiometry of the two photosystems is adjusted and optimized in response to different light quality conditions. Direct evidence is provided that photosystem stoichiometry adjustments in chloroplasts are a compensation strategy designed to correct unbalanced absorption of light by the two photosystems. Such adjustments allow the plant to maintain a high quantum efficiency of photosynthesis under diverse light quality conditions and constitute acclimation that confers to plants a significant evolutionary advantage over that of a fixed photosystem stoichiometry in thylakoid membranes.
Mycorrhizal enhancement of drought resistance of two woody plant species, loblolly pine (Pinus taeda L.) and rose (Rosa hybrida L. cv. Ferdy), occurred independently of phosphorus nutrition. Mycorrhizae tended to alter root morphology and carbon allocation patterns of shoots and roots. Increased drought resistance of mycorrhizal plants was in part attributed to drought-induced colonization by mycorrhizae and the ability of the mycorrhizal plants to maintain high transpiration rates as a result of greater lateral root formation and lower shoot mass (in ectomycorrhizal loblolly pine), and a higher root/shoot ratio and leaf abscission (in endomycorrhizal roses). Neither the endo- nor ectomycorrhizal symbionts affected osmotic adjustment of droughted plants.
In the present study, leaves of different plant species were girdled by the hot wax collar method to prevent export of assimilates. Photosynthetic activity of girdled and control leaves was evaluated 3 to 7 days later by two methods: (a) carbon exchange rate (CER) of attached leaves was determined under ambient CO(2) concentrations using a closed gas system, and (b) maximum photosynthetic capacity (A(max)) was determined under 3% CO(2) with a leaf disc O(2) electrode. Starch, hexoses, and sucrose were determined enzymically. Typical starch storers like soybean (Glycine max L.) (up to 87.5 milligrams of starch per square decimeter in girdled leaves), cotton (Gossypium hirsutum L.), and cucumber (Cucumis sativus L.) responded to 7 days of girdling by increased (80-100%) stomatal resistance (r(s)) and decreased A(max) (>50%). On the other hand, spinach (Spinacia oleracea L.), a typical sucrose storer (up to 160 milligrams of sucrose per square decimeter in girdled leaves), showed only a slight reduction in CER and almost no change in A(max). Intermediate plants like tomato (Lycopersicon esculentum Mill.), sunflower (Helianthus annuus L.), broad bean (Vicia faba L.), bean (Phaseolus vulgaris L.), and pea (Pisum sativum L.), which upon girdling store both starch and sucrose, responded to the girdle by a considerable reduction in CER but only moderate inhibition of A(max), indicating that the observed reduction in CER was primarily a stomatal response. Both the wild-type tobacco (Nicotiana sylvestris) (which upon girdling stored starch and hexoses) and the starchless mutant (which stored only hexoses, up to 90 milligrams per square decimeter) showed 90 to 100% inhibition of CER and approximately 50% inhibition of A(max). In general, excised leaves (6 days) behaved like girdled leaves of the respective species, showing 50% reduction of A(max) in wild-type and starchless N. sylvestris but only slight decline of A(max) in spinach. The results of the present study demonstrate the possibility of the occurrence of end-product inhibition of photosynthesis in a large number of crop plants. The long-term inhibition of photosynthesis in girdled leaves is not confined to stomatal responses since the A(max) declined up to 50%. The inhibition of A(max) by girdling was strongest in starch storers, but starch itself cannot be directly responsible, because the starchless mutant of N. sylvestris was also strongly inhibited. Similarly, the inhibition cannot be attributed to hexose sugars either, because soybean, cotton, and cucumber are among the plants most strongly inhibited although they do not maintain a large hexose pool. Spinach, a sucrose storer, showed the least inhibition in both girdled and excised leaf systems, which indicates that sucrose is probably not directly responsible for the end-product inhibition of photosynthesis. The occurrence of strong end-product inhibition appears to be correlated with high acid-invertase activity in fully expanded leaves. The inhibition may be related to the nature of soluble sugar metabolism in the extrachloroplastic compartment and may be caused by a metabolite that has different rates of accumulation and turnover in sucrose storers and other plants.
Penicillium pinophilum was isolated from the soil in a commercial strawberry field. The strain readily formed arbuscular mycorrhizae (AM) with the roots of strawberry 'Zoji' (Fragaria x ananassa Duch. CV.) when plants were inoculated with either fresh cultured hyphae or root/soil mixtures. Fresh hyphae, however, resulted in higher amounts of colonization than root/soil inoculum. Compared with uninoculated strawberries, inoculation increased plant dry weight by 31%, as well as nitrogen content (47%), phosphorus content (57%), and photosynthetic rate (71%). AM inoculation also shortened the blossom and ripening date by 3 and 4 days, respectively. This is the first report of a P. pinophilum strain resulting in mycorrhiza with strawberry roots. The significant advantages of this strain are that it is easy to culture and inoculation of plants results in significant growth benefits that may be useful in strawberry production.
The roots of most plants are colonized by symbiotic fungi to form mycorrhiza, which play a critical role in the capture of nutrients from the soil and therefore in plant nutrition. Mycorrhizal Symbiosis is recognized as the definitive work in this area. Since the last edition was published there have been major advances in the field, particularly in the area of molecular biology, and the new edition has been fully revised and updated to incorporate these exciting new developments. . Over 50% new material . Includes expanded color plate section . Covers all aspects of mycorrhiza . Presents new taxonomy . Discusses the impact of proteomics and genomics on research in this area.
The roots of most plants are colonized by symbiotic fungi to form mycorrhiza, which play a critical role in the capture of nutrients from the soil and therefore in plant nutrition. Mycorrhizal Symbiosis is recognized as the definitive work in this area. Since the last edition was published there have been major advances in the field, particularly in the area of molecular biology, and the new edition has been fully revised and updated to incorporate these exciting new developments. . Over 50% new material . Includes expanded color plate section . Covers all aspects of mycorrhiza . Presents new taxonomy . Discusses the impact of proteomics and genomics on research in this area.
Most fungi synthesize siderophores as chelating agents which form soluble complexes with Fe3+ with very high stability constants, thus solubilizing ferric Fe. Ericoid mycorrhizal fungi release ferricrocin or fusigen as the main siderophores. Ferricrocin was also shown to be produced by the ectomycorrhizal fungi, Cenococcum geophilum and Hebeloma crustuliniforme. Arbuscular mycorrhizal fungi are reported to enhance Fe-uptake rates of associated host plants which can be taken as an indication that mycorrhizal siderophores of a yet unknown structure may be involved. Mycorrhizal fungi of orchids were shown to produce as the main siderophores, both well known ferrichrome-type siderophores or the novel linear trishydroxamate basidiochrome.
The structural-functional organization of higher plant chloroplasts has been investigated in relation to the particular light conditions during plant growth. (1) Light intensity variations during growth caused changes in the ratio, in the light-saturated uncoupled rates of electron transport to a Hill oxidant and in the distribution of the chloroplast volume between the membrane and stroma phases. (2) Light quality differences during growth had an effect on the PS II/PS I reaction center ratio and on the chloroplast membrane phase differentiation into grana and stroma thylakoids. Plants grown under far-red-enriched (680–710 nm) illumination contained higher (20–25%) amounts of PS II and simultaneously lower (20–25%) amounts of PS I reaction centers. They also showed a higher grana density along with thicker grana stacks in their chloroplasts. (3) The size of the light-harvesting antenna pool of PS II centers was estimated from the fluorescence time course of 3-(3′,4′-dichlorophenyl)-1,1-dimethylurea-poisoned chloroplasts and was found to be fairly constant (±10%) in spite of the variable PS II/PS I reaction center ratio. The results are compatible with the hypothesis that the structural entities of grana facilitated the centralization and relative concentration increase of a certain group of PS II reaction centers.
summaryActivated charcoal added to artificial growth medium enhances initial association between the mycelium of the desert truffle Terfezia leonis Tul. and the roots of Helianthemum sessiliforum (Defs). Pers. in vitro. This is due, at least in part, to adsorption of iron.
The extent to which water channel transport is responsible for the observed increases in root water flow of ectomycorrhizal plants is reported here.
To examine the contribution of water channel transport to root hydraulic conductance, temperatures in the range 4–20°C and mercuric chloride (HgCl 2 ) were used to study the kinetics of water transport in ectomycorrhizal and nonmycorrhizal roots of American elm ( Ulmus americana ) seedlings.
Hydraulic conductance declined with decreasing temperatures in both mycorrhizal and nonmycorrhizal seedlings. However, hydraulic conductance and conductivity were higher in the mycorrhizal than the nonmycorrhizal roots at all temperatures studied. Mercuric chloride had a relatively greater impact on root hydraulic conductance in nonmycorrhizal than mycorrhizal roots and activation energy for root hydraulic conductance was significantly higher in mycorrhizal than nonmycorrhizal plants.
The results suggest that ectomycorrhizal hyphae increase hydraulic conductance of roots by decreasing water flow resistance of the apoplast rather than by water channel‐mediated transport. The high rates of hydraulic conductance at low root temperatures might be important to plants growing in cold soils and under other challenging environmental conditions that inhibit metabolism and limit water transport.
Nutrient transport, namely absorption from the soil solution as well as nutrient transfer from fungus to plant and carbon movement from plant to fungus are key features of mycorrhizal symbiosis. This review summarizes our current understanding of nutrient transport processes in ectomycorrhizal fungi and ectomycorrhizas. The identification of nutrient uptake mechanisms is a key issue in understanding nutrition of ectomycorrhizal plants. With the ongoing functional analysis of nutrient transporters, identified during sequencing of fungal and tree genomes, a picture of individual transport systems should be soon available, with their molecular functions assessed by functional characterization in, e.g., yeast mutant strains or Xenopus oocytes. Beyond the molecular function, systematic searches for knockout mutants will allow us to obtain a full understanding of the role of the individual transporter genes in the physiology of the symbionts. The mechanisms by which fungal and plant cells obtain, process and integrate information regarding nutrient levels in the external environment and the plant demand will be analyzed.
Studies examined net photosynthesis (Pn) and dry matter production of mycorrhizal and nonmycorrhizalPinus taeda at 6 intervals over a 10-month period. Pn rates of mycorrhizal plants were consistently greater than nonmycorrhizal plants, and at 10 months were 2.1-fold greater. Partitioning of current photosynthate was examined by pulse-labelling with14CO2 at each of the six time intervals. Mycorrhizal plants assimilated more14CO2, allocated a greater percentage of assimilated14C to the root systems, and lost a greater percentage of14C by root respiration than did nonmycorrhizal plants. At 10 months, the quantity of14CO2 respired by roots per unit root weight was 3.6-fold greater by mycorrhizal than nonmycorrhizal plants. Although the stimulation of photosynthesis and translocation of current photosynthate to the root system by mycorrhiza formation was consistent with the source-sink concept of sink demand, foliar N and P concentrations were also greater in mycorrhizal plants.
Further studies examined Pn and dry matter production ofPinus contorta in response to various combinations of N fertilization (3, 62, 248 ppm), irradiance and mycorrhizal fungi inoculation. At 16 weeks of age, 6 weeks following inoculation with eitherPisolithus tinctorius orSuillus granulatus, Pn rates and biomass were significantly greater in mycorrhizal than nonmycorrhizal plants. Mycorrhizal plants had significantly greater foliar %P, but not %N, than did nonmycorrhizal plants. Fertilization with 62 ppm N resulted in greater mycorrhiza formation than either 3 or 248 ppm. Increased irradiance resulted in increased mycorrhiza formation.
Vesicular-arbuscular mycorrhizal fungi can affect the water balance of both amply watered and droughted host plants. This
review summarizes these effects and possible causal mechanisms. Also discussed are host drought resistance and the influence
of soil drying on the fungi.
Spore populations of vesicular-arbuscular mycorrhizal (VAM) fungi and formation of mycorrhizae in maize (Zea mays L.) and soybean (Glycine max (L.) Merr.) were studied in three farming systems: a conventional maize-soybean rotation and two low-input systems. Spore populations were counted in soil samples obtained at planting and after harvest for two growing seasons. Maize and soybean root systems were sampled for mycorrhizae early in the growing season. Low-input plots tended to have higher populations of spores of VAM fungi than conventionally farmed plots. Further, the readily identifiable species Gigaspora gigantea (Nicol. & Gerd.) Gerdemann & Trappe, was more numerous in low-inputs plots (up to 30 spores 50 cm−3 soil) than in conventional plots (0–0.3 spores 50 cm−3 soil), suggesting farming system affected species distribution as well. Colonization of plants in the field did not always reflect VAM fungus spore populations at planting. Greenhouse bioassays showed 2.5–10 fold greater colonization of plants growing in soil from low-input than conventional systems. The results indicate that conventional farming systems yield lower levels of VAM fungi whereas low-input sustainable agriculture, with cover crops planted between cash crops, has greater populations of VAM fungi and potential to utilize the benefits of VA mycorrhizae.
Rhizobial and arbuscular mycorrhizal (AM) symbioses each may consume 4–16% of recently photosynthetically-fixed carbon to maintain their growth, activity and reserves. Rhizobia and AM fungi improve plant photosynthesis through N and P acquisition, but increased nutrient uptake by these symbionts does not fully explain observed increases in the rate of photosynthesis of symbiotic plants. In this paper, we test the hypothesis that carbon sink strength of rhizobial and AM symbioses stimulates the rates of photosynthesis. Nutrient-independent effects of rhizobial and AM symbioses result in direct compensation of C costs at the source. We calculated the response ratios of photosynthesis and nutrient mass fraction in the leaves of legumes inoculated with rhizobial and/or AM fungi relative to non-inoculated plants in a number of published studies. On average, photosynthetic rates were significantly increased by 28 and 14% due to rhizobial and AM symbioses, respectively, and 51% due to dual symbiosis. The leaf P mass fraction was increased significantly by 13% due to rhizobial symbioses. Although the increases were not significant, AM symbioses increased leaf P mass fraction by 6% and dual symbioses by 41%. The leaf N mass fraction was not significantly affected by any of the rhizobial, AM and dual symbioses. The rate of photosynthesis increased substantially more than the C costs of the rhizobial and AM symbioses. The inoculation of legumes with rhizobia and/or AM fungi, which resulted in sink stimulation of photosynthesis, improved the photosynthetic nutrient use efficiency and the proportion of seed yield in relation to the total plant biomass (harvest index). Sink stimulation represent an adaptation mechanism that allows legumes to take advantage of nutrient supply from their microsymbionts without compromising the total amount of photosynthates available for plant growth.
Soil humidity and bulk water transport are essential for nutrient mobilization. Ectomycorrhizal fungi, bridging soil and fine roots of woody plants, are capable of modulating both by being integrated into water movement driven by plant transpiration and the nocturnal hydraulic lift. Aquaporins are integral membrane proteins that function as gradient-driven water and/or solute channels. Seven aquaporins were identified in the genome of the ectomycorrhizal basidiomycete Laccaria bicolor and their role in fungal transfer processes was analyzed. Heterologous expression in Xenopus laevis oocytes revealed relevant water permeabilities for three aquaporins. In fungal mycelia, expression of the corresponding genes was high compared with other members of the gene family, indicating the significance of the respective proteins for plasma membrane water permeability. As growth temperature and ectomycorrhiza formation modified gene expression profiles of these water-conducting aquaporins, specific roles in those aspects of fungal physiology are suggested. Two aquaporins, which were highly expressed in ectomycorrhizas, conferred plasma membrane ammonia permeability in yeast. This indicates that these proteins are an integral part of ectomycorrhizal fungus-based plant nitrogen nutrition in symbiosis.
To acquire iron, all species have to overcome the problems of iron insolubility and toxicity. In response to low iron availability in the environment, most fungi excrete ferric iron-specific chelators--siderophores--to mobilize this metal. Siderophore-bound iron is subsequently utilized via the reductive iron assimilatory system or uptake of the siderophore-iron complex. Furthermore, most fungi possess intracellular siderophores as iron storage compounds. Molecular analysis of siderophore biosynthesis was initiated by pioneering studies on the basidiomycete Ustilago maydis, and has progressed recently by characterization of the relevant structural and regulatory genes in the ascomycetes Aspergillus nidulans and Neurospora crassa. In addition, significant advances in the understanding of utilization of siderophore-bound iron have been made recently in the yeasts Saccharomyces cerevisiae and Candida albicans as well as in the filamentous fungus A. nidulans. The present review summarizes molecular details of fungal siderophore biosynthesis and uptake, and the regulatory mechanisms involved in control of the corresponding genes.
The formation of ectomycorrhizas, a tight association between fine roots of trees and certain soil fungi, improves plant nutrition in a nutrient-limited environment and may increase plant survival under water stress conditions. To investigate the impact of mycorrhiza formation on plant water uptake, seven genes coding for putative water channel proteins (aquaporins) were isolated from a poplar ectomycorrhizal cDNA library. Four out of the seven genes were preferentially expressed in roots. Mycorrhiza formation resulted in an increased transcript level for three of these genes, two of which are the most prominently expressed aquaporins in roots. When expressed in Xenopus laevis oocytes, the corresponding proteins of both genes were able to transport water. Together, these data indicate, that the water transport capacity of the plasma membrane of root cells is strongly increased in mycorrhized plants. Measurements of the hydraulic conductance of intact root systems revealed an increased water transport capacity of mycorrhized poplar roots. These data, however, also indicate that changes in the properties of the plasma membrane as well as those of the apoplast are responsible for the increased root hydraulic conductance in ectomycorrhizal symbiosis.
Arbuscular mycorrhizal symbioses have a significant impact on plant interactions with other organisms. Increased resistance to soil-borne pathogens has been widely described in mycorrhizal plants. By contrast, effects on shoot diseases largely rely on the lifestyle and challenge strategy of the attacker. Among the potential mechanisms involved in the resistance of mycorrhizal systems, the induction of plant defenses is the most controversial. During mycorrhiza formation, modulation of plant defense responses occurs, potentially through cross-talk between salicylic acid and jasmonate dependent signaling pathways. This modulation may impact plant responses to potential enemies by priming the tissues for a more efficient activation of defense mechanisms.
Water reactions, drought and vesicular-arbuscular mycorrhizal symbiosis
The aquaporin gene family of the ectomycorrhizal fungus Laccaria bicolor: lessons for symbiotic functions
- S Dietz
- Von Below
- J Beitz
- E Nehls
Dietz S, von Below J, Beitz E, Nehls U (2011) The aquaporin gene family of the ectomycorrhizal
fungus Laccaria bicolor: lessons for symbiotic functions. New Phytol 190:927-940
- E Hacskaylo
Hacskaylo E (1971) Mycorrhizae. U.S. Government Printing Office, Washington, DC, p 255.
ISBN 0-409-068
Mycorrhizal symbiosis. Academic, New York Haselwandter K (2008) Structure and function of siderophores produced by mycorrhizal fungi
- J L Harley
- S E Smith
Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic, New York
Haselwandter K (2008) Structure and function of siderophores produced by mycorrhizal fungi.
Mineral Magazine 77:61-64
Ectomycorrhizas increase apoplastic water transport and root hydraulic conductivity in Ulmus Americana seedlings
- T M Mushin
- J J Zwiazek
Mushin TM, Zwiazek JJ (2002) Ectomycorrhizas increase apoplastic water transport and root
hydraulic conductivity in Ulmus Americana seedlings. New Phytol 153:153-158