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Influence of arbuscular mycorrhizal fungi on the functional mechanisms associated with drought tolerance in carob (Ceratonia siliqua L.)

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Key message Arbuscular mycorrhizal symbiosis strengthened the mechanisms developed by carob to withstand drought stress, including improved water relations, increased cell wall rigidity and osmolytes accumulation, and enhanced oxidative stress alleviation. Abstract The present investigation was carried out to provide more insight into the influence of arbuscular mycorrhizal fungi (Funneliformis mosseae, Rhizophagus fasciculatus, and Rhizophagus intraradices) on drought tolerance of carob. Non-mycorrhizal (NM) and arbuscular mycorrhizal (AM) carob plants were subjected to two watering regimes, 75% of field capacity (well water) or 25% of field capacity (water stress). Obtained results showed that stressed AM plants exhibited increased performance in terms of growth and biomass production, water and nutrient acquisition, and oxidative stress alleviation compared to NM plants. In fact, under limited water regime, AM plants maintained high stomatal conductance and high relative water content (over 94%) due to their high water and nutrient uptake efficiency. Moreover, AM plants especially those associated with F. mosseae maintained high membrane integrity (over 80%), high cell wall rigidity, and high leaf water potential and osmotic potential at full turgor and at turgor loss, while these parameters steeply decreased in NM plants. Furthermore, drought-stressed AM plants showed decreased hydrogen peroxide and malondialdehyde contents associated with increased activities of superoxide dismutase, ascorbate peroxidase, guaiacol peroxidase, and catalase compared to their relative NM plants. Thus, AMF strengthened the mechanisms involved in drought tolerance of carob by improving water relations, increasing cell wall rigidity, and enhancing oxidative stress alleviation. Funneliformis mosseae was the most effective in improving carob tolerance to drought stress.
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Vol.:(0123456789)
1 3
Trees (2018) 32:87–97
DOI 10.1007/s00468-017-1613-8
ORIGINAL ARTICLE
Influence ofarbuscular mycorrhizal fungi onthefunctional
mechanisms associated withdrought tolerance incarob
(Ceratonia siliqua L.)
AbdellatifEssahibi1· LailaBenhiba1· MohamedAitBabram2· CherkiGhoulam1·
AhmedQaddoury1
Received: 7 April 2017 / Accepted: 1 September 2017 / Published online: 9 September 2017
© Springer-Verlag GmbH Germany 2017
drought-stressed AM plants showed decreased hydrogen
peroxide and malondialdehyde contents associated with
increased activities of superoxide dismutase, ascorbate per-
oxidase, guaiacol peroxidase, and catalase compared to their
relative NM plants. Thus, AMF strengthened the mecha-
nisms involved in drought tolerance of carob by improving
water relations, increasing cell wall rigidity, and enhanc-
ing oxidative stress alleviation. Funneliformis mosseae was
the most effective in improving carob tolerance to drought
stress.
Keywords Ceratonia siliqua· Arbuscular mycorrhizal
fungi· Drought stress· Water relations· Antioxidant
metabolism· Osmotic adjustment
Introduction
Carob (Ceratonia siliqua L.) tree is an important compo-
nent of the arboreal flora of the Mediterranean regions,
where it is widely cultivated for economic, environmen-
tal, and social benefits (Batlle and Tous 1997). Indeed,
seeds and pods of carob are used in food, pharmaceutical,
chemical, and cosmetic industries (Makris and Kefalas
2004; Barracosa etal. 2007; Konate 2007; Custodio etal.
2011a, b). In addition, carob tree plays a key role in the
conservation and rehabilitation of marginal areas of Med-
iterranean basin, where it plays the role of pioneer and
productive species. Carob can also be used for charcoal,
wood industry, and to prevent soil erosion (Barwick 2004;
Pérez-García 2009). Several studies reported the capacity
of carob tree to tolerate dryness and salinity and to adapt
to nutrient poor and degraded soils (Vertovec etal. 2001;
Sakcali and Ozturk 2004; Correia etal. 2010; Ozturk
etal. 2010; El-Refaey etal. 2011; El Asri etal. 2013,
Abstract
Key message Arbuscular mycorrhizal symbiosis
strengthened the mechanisms developed by carob to
withstand drought stress, including improved water rela-
tions, increased cell wall rigidity and osmolytes accumu-
lation, and enhanced oxidative stress alleviation.
Abstract The present investigation was carried out to pro-
vide more insight into the influence of arbuscular mycor-
rhizal fungi (Funneliformis mosseae, Rhizophagus fascicu-
latus, and Rhizophagus intraradices) on drought tolerance
of carob. Non-mycorrhizal (NM) and arbuscular mycorrhizal
(AM) carob plants were subjected to two watering regimes,
75% of field capacity (well water) or 25% of field capacity
(water stress). Obtained results showed that stressed AM
plants exhibited increased performance in terms of growth
and biomass production, water and nutrient acquisition, and
oxidative stress alleviation compared to NM plants. In fact,
under limited water regime, AM plants maintained high
stomatal conductance and high relative water content (over
94%) due to their high water and nutrient uptake efficiency.
Moreover, AM plants especially those associated with F.
mosseae maintained high membrane integrity (over 80%),
high cell wall rigidity, and high leaf water potential and
osmotic potential at full turgor and at turgor loss, while these
parameters steeply decreased in NM plants. Furthermore,
Communicated by P. E. Courty.
* Abdellatif Essahibi
abdellatif.essahibi@gmail.com
1 Department ofBiology, Faculty ofSciences andTechniques,
Cadi Ayyad University, Marrakesh, Morocco
2 Department ofMathematics, Faculty ofSciences
andTechniques, Cadi Ayyad University, Marrakesh,
Morocco
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In recent years, the application of arbuscular mycorrhizal fungi (AMF) has been considered to be an important strategy for improving crop yield and quality. In the present study, a factorial experiment based on a complete randomized design with two factors was performed to investigate the effect of AMF and water stress on the essential oil (EO) composition, antioxidant activity, and physiological and morphological characteristics of rose-scented geranium (Pelargonium graveolens L.). The factors included AMF inoculation (Rhizophagus intraradices, Funneliformis mosseae, and a mixture of both species) and irrigation levels [well-watered (WW), moderate drought stress (MDS), and severe drought stress (SDS)]. The main EO constituents were citronellol (31–37%) and geraniol (9–14%) in all treatments. Under water-stress conditions, some constituents increased, such as geraniol and geranyl formate, whereas others decreased, such as linalool, menthone and rose oxide. Overall, the highest amount of citronellol (37.3%) and geraniol (14.8%) was obtained in the plants inoculated with F. mosseae and R. intraradices under WW and MDS conditions, respectively. Antioxidant activity, total flavonoids, and phenolics were increased because of AMF inoculation, whereas a different trend was observed for the phenolic and flavonoid contents under water-stress conditions. Furthermore, water deficit elevated the amount of soluble carbohydrates as well as the proline content, whereas the amount of proline was lower in inoculated plants than in non-inoculated ones. All the growth parameters were improved in the AMF-inoculated plants compared to non-inoculated ones under different irrigation regimes. Drought conditions decreased the photosynthetic pigments and efficiency, whereas AMF plants ameliorated the adverse effect of drought conditions. In general, mycorrhizal inoculation resulted in an improvement in the growth parameters as well as the phytochemical and physiological characteristics of rose-scented geranium.
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The present investigation was undertaken to improve the performance of carob cuttings in terms of adventitious roots formation and hardening using arbuscular mycorrhizal fungi (AMF). Softwood cuttings were treated with 5000 mg L-1 of indole-3-butyric acid (IBA) and kept noninoculated (Non-AM) or inoculated with Funneliformis mosseae (Fmo) alone or combined with Rhizophagus fasciculatus (Fmo+Rfa) or R. intraradices (Fmo+Rin) or both (Fmo+Rfa+Rin) and then maintained under mist conditions. After two months, rooted cuttings were transplanted on sterilized substrate and transferred to a hardening greenhouse for five months. Obtained results showed that inoculation of the rooting substrate with AMF substantially improved the percentage of rooted cuttings and the number of roots per cutting. The highest rooting (63.33%) and number of roots per cutting (11.67) were recorded in the presence of the complex of the three AMF strains (Fmo+Rfa+Rin). Moreover, all mycorrhizal-rooted cuttings survived transplantation and hardening shocks and showed the highest growth and physiological performances. Indeed, in the Fmo-Rfa-Rin-plantlets the gains in plant height and shoot and root dry weights were 95.6%, 55.1% and 76.9% respectively. Furthermore, stomatal conductance, total chlorophyll content, photochemical efficiency of PSII (Fv/Fm) and nutrient concentrations were higher in mycorrhizal plantlets than in non-AM ones. Thus, AMF substantially improved carob cuttings’ performance in terms of rooting capacity and hardening efficiency, thereby increasing the potential of carob propagation by cuttings.
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The effects of presence and absence of arbuscular mycorrhizal (AM+ and AM-) fungus Glomus intraradices on agronomic and chemical characteristics of field- grown tobacco ( Nicotiana tabacum L.) “Virginia” type (cv. K-326) plants exposed to varying concentrations of chloride 10, 40, 70 and 100 mg Cl L<sup>-1</sup> (C1-C4) were studied over two growing seasons (2012– 2013). Mycorrhizal plants had significantly higher uptake of nutrients in shoots and number of leaves regardless of intensities of chloride stress. The cured leaves yield of AM+ plants under C2-C4 chloride stressed conditions were higher than AM- plants. Leaf chloride content increased in linearly with the increase of chloride level while AMF colonized plants maintained low Cl content. AM+ plants produced tobacco leaves that contain significantly higher quantities of nicotine than AM- plants. AM inoculation ameliorated the chloride stress to some extent. Antioxidant enzymes like superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX) and glutathione reductase (GR) as well as non-enzymatic antioxidants (ascorbic acid and glutathione) also exhibited great variation with chloride treatment. Chloride stress caused great alterations in the endogenous levels of growth hormones with abscisic acid showing increment. AMF inoculated plants maintained higher levels of growth hormones and also allayed the negative impact of chloride. The level of 40 mg L<sup>-1</sup> in combination with arbuscular mycorrhizal can be considered as the acceptable threshold to avoid adverse effects on Virginia tobacco.
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The influence of arbuscular mycorrhizal fungi (AMF) (Glomus spp.) on some physiological and biochemical characteristics of bioenergy grass Saccharum arundinaceum subjected to drought stress was studied. The symbiotic association of Glomus spp. was established with S. arundinaceum, a potential bioenergy grass as evident from the increase in percentage of root infection and distribution frequency of vesicles when compared with non-arbuscular mycorrhizal plants. AMF-treated plants exhibited an enhanced accumulation of osmolytes such as sugars and proline and also increased protein content under drought. AMF association significantly increased the accumulation of non-enzymatic antioxidants like phenols, ascorbate and glutathione as well as enhanced the activities of antioxidant enzymes such as SOD (superoxide dismutase), APX (ascorbate peroxidase) and GPX (guaiacol peroxidase) resulting in reduced lipid peroxidation in S. arundinaceum. AMF symbiosis also ameliorated the drought-induced reduction of total chlorophyll content and activities of photosystem I and II. The maximum quantum efficiency of PS II (F v/F m) and potential photochemical efficiency (F v/F o) were higher in AMF plants as compared to non-AMF plants under drought stress. These results indicate that AMF association alleviate drought stress in S. arundinaceum by the accumulation of osmolytes and non-enzymatic antioxidants and enhanced activities of antioxidant enzymes, and hence, the photosynthetic efficiency is improved resulting in increased biomass production. AMF association with energy grasses also improves the acclimatization of S. arundinaceum for growing in marginal lands of drought-affected soils.
Book
This book reviews the potential mechanisms in arbuscular mycorrhizas (AMs), in the hope that this can help arbuscular mycorrhizal fungi (AMF) to be more used efficiently as a biostimulant to enhance stress tolerance in the host plants. AMF, as well as plants, are often exposed to all or many of the abiotic and biotic stresses, including extreme temperatures, pH, drought, water-logging, toxic metals and soil pathogens. Studies have indicated a quick response to these stresses involving several mechanisms, such as root morphological modification, reactive oxygen species change, osmotic adjustment, direct absorption of water by extraradical hyphae, up-regulated expression of relevant stressed genes, glomalin-related soil protein release, etc. The underlying complex, multi-dimensional strategy is involved in morphological, physiological, biochemical, and molecular processes. The AMF responses are often associated with homeostatic regulation of the internal and external environment, and are therefore critical for plant health, survival and restoration in native ecosystems and good soil structure. © Springer Nature Singapore Pte Ltd. 2017. All rights reserved.
Article
The differential influence of arbuscular mycorrhiza- Rhizophagus intraradices (Ri) and endophyte- Piriformospora indica (Pi) on drought tolerance in finger millet was studied. The seedlings were grown with and without symbiotic association under three different water regimes and the effect of association on physiological and biochemical traits related to stress tolerance were recorded. The treated plants exhibited an enhanced seedlings growth under drought, while Ri seedlings had greater plant biomass as compared to endophytic fungi. Chlorophyll and relative water content were significantly increased in Pi inoculated plants. Ri was more effective in reducing the electrolyte leakages, malondialdehyde (MDA) and hydrogen peroxide (H2O2) content as compare to control and Pi treatments. Proline content in leaves increased significantly with Ri and Pi, but Ri treated plants accumulated more total soluble sugars as compared to inoculated seedlings. In case of secondary metabolites, phenols accumulation was influenced by both Ri and Pi under water stress, while more flavonoids were present in Ri seedlings. Also Pi showed better performance with respect to improved Ascorbate-glutathione redox status under mild and severe stress. Both symbionts differentially enhanced the activities of the antioxidant enzymes resulting in upto 25% reduction in drought-induced lipid peroxidation. Obtained results indicated that, inoculation with both fungi helped finger millet seedlings in drought tolerance through a stronger antioxidant defence system, higher chlorophyll content, and an enriched osmoregulatory network. Both Ri and Pi fungi may differ in their biochemical and genetic mechanisms behind the interaction; however can improve the growth of finger millet in drought-affected soils.