Juan Manuel Ruiz-Lozano

Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies.

Water deficit is considered one of the most important abiotic factors limiting plant growth and yield in many areas on earth. Several eco-physiological studies have demonstrated that the arbuscular mycorrhizal (AM) symbiosis often results in altered rates of water movement into, through and out of the host plants, with consequent effects on tissue hydration and plant physiology. It is now accepted that the contribution of AM symbiosis to plant drought tolerance is the result of accumulative physical, nutritional, physiological and cellular effects. This review considers several aspects that should be investigated at a molecular level in order to gain a whole understanding of the different mechanisms by which the AM symbiosis protects the host plants against the detrimental effects of water deficit.

Regulation of root water uptake under abiotic stress conditions

A common effect of several abiotic stresses is to cause tissue dehydration. Such dehydration is caused by the imbalance between root water uptake and leaf transpiration. Under some specific stress conditions, regulation of root water uptake is more crucial to overcome stress injury than regulation of leaf transpiration. This review first describes present knowledge about how water is taken up by roots and then discusses how specific stress situations such as drought, salinity, low temperature, and flooding modify root water uptake. The rate of root water uptake of a given plant is the result of its root hydraulic characteristics, which are ultimately regulated by aquaporin activity and, to some extent, by suberin deposition. Present knowledge about the effects of different stresses on these features is also summarized. Finally, current findings regarding how molecular signals such as the plant hormones abscisic acid, ethylene, and salicylic acid, and how reactive oxygen species may modulate the final response of root water uptake under stress conditions are discussed.

Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies

Excessive salt accumulation in soils is a major ecological and agronomical problem, in particular in arid and semi-arid areas. Excessive soil salinity affects the establishment, development, and growth of plants, resulting in important losses in productivity. Plants have evolved biochemical and molecular mechanisms that may act in a concerted manner and constitute the integrated physiological response to soil salinity. These include the synthesis and accumulation of compatible solutes to avoid cell dehydration and maintain root water uptake, the regulation of ion homeostasis to control ion uptake by roots, compartmentation and transport into shoots, the fine regulation of water uptake and distribution to plant tissues by the action of aquaporins, the reduction of oxidative damage through improved antioxidant capacity and the maintenance of photosynthesis at values adequate for plant growth. Arbuscular mycorrhizal (AM) symbiosis can help the host plants to cope with the detrimental effects of high soil salinity. There is evidence that AM symbiosis affects and regulates several of the above mentioned mechanisms, but the molecular bases of such effects are almost completely unknown. This review summarizes current knowledge about the effects of AM symbiosis on these physiological mechanisms, emphasizing new perspectives and challenges in physiological and molecular studies on salt-stress alleviation by AM symbiosis.

Salinity stress alleviation using arbuscular mycorrhizal fungi. A review

Salinity is one of the most severe environmental stress as it decreases crop production of more than 20% of irrigated land worldwide. Hence, it is important to develop salt-tolerant crops. Understanding the mechanisms that enable plant growth under saline conditions is therefore required. Acclimation of plants to salinized conditions depends upon activation of cascades of molecular networks involved in stress sensing, signal transduction, and the expression of specific stress-related genes and metabolites. The stress signal is first perceived at the membrane level by the receptors and then transduced in the cell to switch on the stress-responsive genes which mediate stress tolerance. In addition to stress-adaptative mechanisms developed by plants, arbuscular mycorrhizal fungi have been shown to improve plant tolerance to abiotic environmental factors such as salinity. In this review, we emphasize the significance of arbuscular mycorrhizal fungi alleviation of salt stress and their beneficial effects on plant growth and productivity. Although salinity can affect negatively arbuscular mycorrhizal fungi, many reports show improved growth and performance of mycorrhizal plants under salt stress conditions. These positive effects are explained by improved host plant nutrition, higher K+/Na+ ratios in plant tissues and a better osmotic adjustment by accumulation of compatible solutes such as proline, glycine betaine, or soluble sugars. Arbuscular mycorrhizal plants also improve photosynthetic- and water use efficiency under salt stress. Arbuscular mycorrhizal plants enhance the activity of antioxidant enzymes in order to cope with the reactive oxygen species generated by salinity. At the molecular level, arbuscular mycorrhizal symbiosis regulates the expression of plant genes involved in the biosynthesis of proline, of genes encoding aquaporins, and of genes encoding late embryogenesis abundant proteins, with chaperone activity. The regulation of these genes allows mycorrhizal plants to maintain a better water status in their tissues. Gene expression patterns suggest that mycorrhizal plants are less strained by salt stress than non-mycorrhizal plants. In contrast, scarce information is available on the possible regulation by the arbuscular mycorrhizal symbiosis of plant genes encoding Na+/H+ antiporters or cyclic nucleotide-gated channels. These genes encode proteins with a key role in the regulation of uptake, distribution and compartimentation of sodium and other ions within the plant, and are major determinants for the salt sensitiveness of a plant. Thus, we propose that investigating the participation of cation proton antiporters and cyclic nucleotide-gated channels on arbuscular mycorrhizal symbiosis under salinity is a promising field that should shed further light on new mechanisms involved in the enhanced tolerance of mycorrhizal plants to salt stress.

Symbiotic efficiency and infectivity of an autochthonous arbuscular mycorrhizal Glomus sp. from saline soils and Glomus deserticola under salinity.

Abstract The purpose of this study was to compare the effect of salinity on the symbiotic efficiencies and mycelial infectivity of two arbuscular mycorrhizal fungi (AMF), one isolated from saline soils (Glomus sp.) and the other (Glomus deserticola) from nonsaline soils (belonging to the Estación Experimental del Zaidín collection). Lettuce plants inoculated with either of these two fungi or maintained as uninoculated controls were grown in soil with three salt concentrations (0.25, 0.50 or 0.75 g NaCl kg–1 dry soil). Both AMF protected host plants against salinity. However, when the results of shoot dry weight and nutrient contents were expressed relative to the total length of mycorrhiza formed, it was found that both AMF differed in their symbiotic efficiencies. These differences were more evident at the two highest salt levels. Glomus sp.-colonized plants grew less and accumulated less N and P, whereas they formed a higher amount of mycorrhiza. The mechanism by which Glomus sp. protected plants from the detrimental effects of salt was based on the stimulation of root development, while the effects of G. deserticola were based on improved plant nutrition. The increase in salinity of soil decreased the hyphal growth and/or viability of Glomus sp. to a higher extent than those of G. deserticola since the mycelial network generated by G. deserticola was more infective than that of Glomus sp.

PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance

Although the discovery of aquaporins in plants has resulted in a paradigm shift in the understanding of plant water relations, the relationship between aquaporins and plant responses to drought still remains elusive. Moreover, the contribution of aquaporin genes to the enhanced tolerance to drought in arbuscular mycorrhisal (AM) plants has never been investigated. Therefore, we studied, at a molecular level, whether the expression of aquaporin-encoding genes in roots is altered by the AM symbiosis as a mechanism to enhance host plant tolerance to water deficit. In this study, genes encoding plasma membrane aquaporins (PIPs) from soybean and lettuce were cloned and their expression pattern studied in AM and nonAM plants cultivated under well-watered or drought stressed conditions. Results showed that AM plants responded to drought stress by down-regulating the expression of the PIP genes studied and anticipating its down-regulation as compared to nonAM plants. The possible physiological implications of this down-regulation of PIP genes as a mechanism to decrease membrane water permeability and to allow cellular water conservation is further discussed.

Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants.

Arbuscular mycorrhizal (AM) symbiosis can alleviate salt stress in plants. However the intimate mechanisms involved, as well as the effect of salinity on the production of signalling molecules associated to the host plant-AM fungus interaction remains largely unknown. In the present work, we have investigated the effects of salinity on lettuce plant performance and production of strigolactones, and assessed its influence on mycorrhizal root colonization. Three different salt concentrations were applied to mycorrhizal and non-mycorrhizal plants, and their effects, over time, analyzed. Plant biomass, stomatal conductance, efficiency of photosystem II, as well as ABA content and strigolactone production were assessed. The expression of ABA biosynthesis genes was also analyzed. AM plants showed improved growth rates and a better performance of physiological parameters such as stomatal conductance and efficiency of photosystem II than non-mycorrhizal plants under salt stress since very early stages - 3 weeks - of plant colonization. Moreover, ABA levels were lower in those plants, suggesting that they were less stressed than non-colonized plants. On the other hand, we show that both AM symbiosis and salinity influence strigolactone production, although in a different way in AM and non-AM plants. The results suggest that AM symbiosis alleviates salt stress by altering the hormonal profiles and affecting plant physiology in the host plant. Moreover, a correlation between strigolactone production, ABA content, AM root colonization and salinity level is shown. We propose here that under these unfavourable conditions, plants increase strigolactone production in order to promote symbiosis establishment to cope with salt stress.

Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery

The arbuscular mycorrhizal (AM) symbiosis enhances plant tolerance to water deficit through the alteration of plant physiology and the expression of plant genes. These changes have been postulated to be caused (among others) by different contents of abscisic acid (ABA) between AM and non-AM plants. However, there are no studies dealing with the effects of exogenous ABA on the expression of stress-related genes and on the physiology of AM plants. The aim of the present study was to evaluate the influence of AM symbiosis and exogenous ABA application on plant development, physiology, and expression of several stress-related genes after both drought and a recovery period. Results show that the application of exogenous ABA had contrasting effects on AM and non-AM plants. Only AM plants fed with exogenous ABA maintained shoot biomass production unaltered by drought stress. The addition of exogenous ABA enhanced considerably the ABA content in shoots of non-AM plants, concomitantly with the expression of the stress marker genes Lsp5cs and Lslea and the gene Lsnced. By contrast, the addition of exogenous ABA decreased the content of ABA in shoots of AM plants and did not produce any further enhancement of the expression of these three genes. AM plants always exhibited higher values of root hydraulic conductivity and reduced transpiration rate under drought stress. From plants subjected to drought, only the AM plants recovered their root hydraulic conductivity completely after the 3 d recovery period. As a whole, the results indicate that AM plants regulate their ABA levels better and faster than non-AM plants, allowing a more adequate balance between leaf transpiration and root water movement during drought and recovery.

The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress.

Rice (Oryza sativa) is the most important crop for human consumption, providing staple food for more than half of the worlds population. Rice is conventionally grown under flooded conditions for most of its growing cycle. However, about half of the rice area in the world does not have sufficient water to maintain optimal growing conditions and yield is reduced by drought. One possible way to increase rice production in order to meet the rice demand is to improve its drought tolerance by means of the arbuscular mycorrhizal (AM) symbiosis. Thus, AM and non-AM rice plants were maintained under well-watered conditions or were subjected to moderate and severe drought stress for 15d. After that, half of the plants from each treatment were harvested, while the other half were allowed to recover from drought for additional 25d. The results showed that rice can benefit from the AM symbiosis and improve their long-term development after a drought stress period. In fact, at each watering level, AM plants showed about 50% enhanced shoot fresh weight as compared to non-AM plants. The AM symbiosis enhanced the plant photosynthetic efficiency under stress over 40%, induced the accumulation of the antioxidant molecule glutathione and reduced the accumulation of hydrogen peroxide and the oxidative damage to lipids in these plants. Thus, these combined effects enhanced the plant performance after a drought stress period.

Defense Genes Are Differentially Induced by a Mycorrhizal Fungus and Rhizobium sp. in Wild-Type and Symbiosis-Defective Pea Genotypes

Mycorrhiza-resistant and non-nodulating pea mutants provide a model system for identifying common genes regulated during the early events in mycorrhiza and nodule establishment. Inoculation of pea roots with Glomus mosseae or Rhizobium leguminosarum can induce overex-pression of seven defense-related genes (pI 206, pI 49, pI 176, PR 10, basic A1-chitinase, transcinnamic acid 4-hydroxylase, chalcone isomerase), depending on the plant genotype and the time point of interaction between the plant and the microsymbiont. Expression of the pI 206 gene is closely correlated with appressorium formation by the mycorrhizal fungus on both mutant and wild-type pea roots. The gene is also induced by the pathogen Aphanomyces euteiches. Transcript accumulation was higher in mutant than in wild-type genotypes for five and six of the studied genes during early stages of root interactions with G. mosseae and R. leguminosarum, respectively, and this is discussed in relation to the symbiotic-defective phenotype of Myc-1Nod¯ p...