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Rhizosphere Microbes as Essential Partners for Plant Stress Tolerance

2013; Elsevier BV; Volume: 6; Issue: 2 Linguagem: Inglês

10.1093/mp/sst028

1674-2052

Axel de Zélicourt, Mohamed S. Alyousif, Heribert Hirt,

Mycorrhizal Fungi and Plant Interactions

Ever since plants colonized land, they evolved mechanisms to respond to changing environmental conditions and settle in extreme habitats. Recent studies show that several plant species require microbial associations for stress tolerance and survival. Although many plants lack the adaptive capability to adapt to stress conditions, the ability of a variety of plants to adapt to stress conditions often appears to depend on their association with certain microbes, raising a number of questions: What distinguishes the microbes and plants that can adapt to extreme environmental conditions? Can all plants improve stress tolerance when associated with appropriate microbial partners? Answers to these questions should modify our concepts of plant physiology and could lead to new ways towards a sustainable agriculture. Due to their sessile nature, plants have always been confronted with various abiotic and biotic stresses in their immediate environment. As a consequence, the survival of plants depends on their ability to rapidly adjust their physiology, development, and growth to escape or mitigate the impacts of stress. All plants are known to perceive and respond to stress signals such as drought, heat, salinity, herbivory, and pathogens (Hirt, 2009Hirt H Plant Stress Biology: From Genomics to Systems Biology. Wiley, West Sussex2009Crossref Scopus (16) Google Scholar). Some responses are common to various stresses, including the production of certain proteins and the adjustment of the primary metabolism. Due to photosynthesis, plants can produce carbohydrates, of which a considerable fraction passes to root-associated microorganisms, commonly denoted as the rhizosphere. Plant growth also requires significant quantities of nitrate, phosphate, and other minerals which are often not available in free form or in limited quantities in the soil. This is where root-associated beneficial microbes are important partners. The best-known beneficial microbes are mycorrhizal fungi and rhizobia. Approximately 80% of all terrestrial plant species interact with mycorrhiza which make phosphate and nitrate available to plants. Free-living or endophytic rhizobia can fix atmospheric nitrogen, but only the family of leguminosae profits from such an interaction through their ability to house rhizobia in root nodules. The interaction of plants with mycorrhizal fungi and rhizobial bacteria is well documented (Corradi and Bonfante, 2012Corradi N. Bonfante P The arbuscular mycorrhizal symbiosis: origin and evolution of a beneficial plant infection.PLoS Pathog. 2012; 8: e1002600Crossref PubMed Scopus (69) Google Scholar; Geurts et al., 2012Geurts R. Lillo A. Bisseling T Exploiting an ancient signalling machinery to enjoy a nitrogen fixing symbiosis.Curr. Opin. Plant Biol. 2012; 15: 438-443Crossref PubMed Scopus (50) Google Scholar). Non-symbiotic rhizosphere microbes have received much less attention and are therefore treated in this review. Soil-grown plants are immersed in a sea of microbes and diverse beneficial microorganisms such as plant-growth-promoting bacteria (PGPB) as well as plant-growth-promoting fungi (PGPF) can stimulate plant growth and/or confer enhanced resistance to biotic and abiotic stresses (Lugtenberg and Kamilova, 2009Lugtenberg B. Kamilova F Plant-growth-promoting rhizobacteria.Annu. Rev. Microbiol. 2009; 63: 541-556Crossref PubMed Scopus (2254) Google Scholar). The establishment of beneficial plant–microbial interactions requires the mutual recognition and a considerable orchestration of the responses at both the plant and the microbial side. Rhizobial and mycorrhizal symbioses share a common plant-signaling pathway that is activated by rhizobial and mycorrhizal factors (Corradi and Bonfante, 2012Corradi N. Bonfante P The arbuscular mycorrhizal symbiosis: origin and evolution of a beneficial plant infection.PLoS Pathog. 2012; 8: e1002600Crossref PubMed Scopus (69) Google Scholar) and this signaling pathway also seems to be activated by certain beneficial bacteria, suggesting that different beneficial and pathogenic microbes initiate common plant-signaling pathways. Recent evidence indicates that beneficial and pathogenic microbes also suppress the host defense system by various strategies, including the production of effectors, exopolysaccharides, or phytohormones (Zamioudis and Pieterse, 2012Zamioudis C. Pieterse C.M.J Modulation of host immunity by beneficial microbes.Mol. Plant–Microbe Interact. 2012; 25: 139-150Crossref PubMed Scopus (544) Google Scholar). PGPBs belong to a number of different bacterial families, including Rhizobium, Bacillus, Pseudomonas, Burkholderia, etc. PGPBs can improve the growth of vegetables and crops under abiotic stress conditions (Egamberdieva and Kucharova, 2009Egamberdieva D. Kucharova Z Selection for root colonizing bacteria stimulating wheat growth in saline soils.Biol. Fert. Soil. 2009; 45: 563-571Crossref Scopus (213) Google Scholar) and might therefore open new applications for a sustainable agriculture. Enhanced salt tolerance of Zea mays upon co-inoculation with Rhizobium and Pseudomonas is correlated with decreased electrolyte leakage and maintenance of leaf water contents (Bano and Fatima, 2009Bano A. Fatima M Salt tolerance in Zea mays (L.) following inoculation with Rhizobium and Pseudomonas.Biol. Fert. Soils. 2009; 45: 405-413Crossref Scopus (273) Google Scholar). Some microorganisms produce plant hormones, such as indole acetic acid and gibberellic acid, which induce increased root growth and thereby lead to enhanced uptake of nutrients (Egamberdieva and Kucharova, 2009Egamberdieva D. Kucharova Z Selection for root colonizing bacteria stimulating wheat growth in saline soils.Biol. Fert. Soil. 2009; 45: 563-571Crossref Scopus (213) Google Scholar). Plants have the ability to acquire a state of induced systemic resistance (ISR) to pathogens after inoculation with PGPBs. In association with plant roots, PGPBs can prime the plant innate immune system and confer resistance to a broad spectrum of pathogens with a minimal impact on yield and growth (Van Hulten et al., 2006Van Hulten M. Pelser M. Van Loon L.C. Pieterse C.M.J. Ton J Costs and benefits of priming for defense in Arabidopsis.Proc. Natl Acad. Sci. U S A. 2006; 103: 5602-5607Crossref PubMed Scopus (602) Google Scholar). Several PGPBs, including Pseudomonas fluorescens, Pseudomonas putida, Bacillus pumilus, Serratia marcescens, Paenibacillus alvei, Acinetobacter lwoffii, Chryseobacterium balustinum, and Azospirillum brasilense colonize roots and protect on a large variety of plant species, including vegetables, crops, and even trees, against foliar diseases in greenhouse and field trials (Van Loon, 2007Van Loon L.C Plant responses to plant growth-promoting rhizobacteria.European J. Plant Pathol. 2007; 119: 243-254Crossref Scopus (526) Google Scholar). Mycorrhizal and/or endophytic fungi can interact with many plant species and thereby significantly contribute to the adaptation of these plants to a number of environmental stresses (Rodriguez et al., 2008Rodriguez R.J. Henson J. Van Volkenburgh E. Hoy M. Wright L. Beckwith F. Kim Y.O. Redman R.S Stress tolerance in plants via habitat-adapted symbiosis.ISME J. 2008; 2: 404-416Crossref PubMed Scopus (703) Google Scholar). These conditions include drought, heat, pathogens, herbivores, or limiting nutrients. Moreover, some plants are unable to withstand stress conditions in the absence of their associated microbes (Redman et al., 2002Redman R.S. Sheehan K.B. Stout R.G. Rodriguez R.J. Henson J.M Thermotolerance conferred to plant host and fungal endophyte during mutualistic symbiosis.Science. 2002; 298: 1581Crossref PubMed Scopus (542) Google Scholar). It appears that stress tolerance of the host plant can be a habitat-specific feature of the interaction. For example, Curvularia protuberata confers heat tolerance to its geothermal host plant Dichanthelium lanuginosum. However, neither the fungus nor the plant can survive alone at temperatures above 38°C (Redman et al., 2002Redman R.S. Sheehan K.B. Stout R.G. Rodriguez R.J. Henson J.M Thermotolerance conferred to plant host and fungal endophyte during mutualistic symbiosis.Science. 2002; 298: 1581Crossref PubMed Scopus (542) Google Scholar). Moreover, only C. protuberata isolates from geothermal plants can confer heat tolerance (Rodriguez et al., 2008Rodriguez R.J. Henson J. Van Volkenburgh E. Hoy M. Wright L. Beckwith F. Kim Y.O. Redman R.S Stress tolerance in plants via habitat-adapted symbiosis.ISME J. 2008; 2: 404-416Crossref PubMed Scopus (703) Google Scholar). A comparison of different fungal endophytes unravels a further layer of specificity: C. protuberata confers heat but neither disease nor salt tolerance. In contrast, Fusarium culmorum only confers salt tolerance and Curvularia magna only disease tolerance (Rodriguez et al., 2008Rodriguez R.J. Henson J. Van Volkenburgh E. Hoy M. Wright L. Beckwith F. Kim Y.O. Redman R.S Stress tolerance in plants via habitat-adapted symbiosis.ISME J. 2008; 2: 404-416Crossref PubMed Scopus (703) Google Scholar). It appears that these specific features contribute to the ability of some plants to establish and survive in extreme habitats. Symbiotically conferred disease tolerance appears to involve different mechanisms depending on the endophyte. For example, a non-pathogenic Colletotrichum strain that confers disease resistance does not activate host defense in the absence of pathogen challenge (Redman et al., 1999Redman R.S. Freeman S. Clifton D.R. Morrel J. Brown G. Rodriguez R.J Biochemical analysis of plant protection afforded by a nonpathogenic endophytic mutant of Colletotrichum magna.Plant Physiol. 1999; 119: 795-804Crossref PubMed Scopus (110) Google Scholar). Moreover, disease resistance is localized to tissues that the fungus has colonized, but is not systemic. In contrast, Piriformospora indica confers disease resistance systemically. P. indica colonizes the roots of many plant species and stimulates growth, biomass, and seed production of the hosts (Fig. 1). P. indica promotes nitrate and phosphate uptake and confers resistance against abiotic (Waller et al., 2005Waller F. Achatz B. Baltruschat H. Fodor J. Becker K. Fischer M. Heier T. Hückelhoven R. Neumann C. von Wettstein D. Franken P. Kogel K.H The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield.Proc. Natl Acad. Sci. U S A. 2005; 102: 13386-13391Crossref PubMed Scopus (894) Google Scholar) and biotic stress (Stein et al., 2008Stein E. Molitor A. Kogel K.H. Waller F Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1.Plant Cell Physiol. 2008; 49: 1747-1751Crossref PubMed Scopus (210) Google Scholar). Colonization by the fungus stimulates the host to synthesize phosphatidic acid, which triggers the OXI1 pathway (Camehl et al., 2011Camehl I. Drzewiecki C. Vadassery Y. Shahollari B. Sherameti I. Forzani C. Munnik T. Hirt H. Oelmüller R. The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis.PloS Pathog. 2011; 7: e1002051Crossref PubMed Scopus (99) Google Scholar). This pathway is usually activated only in response to pathogen attack to activate host defense (Rentel et al., 2004Rentel M.C. Lecourieux D. Ouaked F. Usher S.L. Petersen L. Okamoto H. Knight H. Peck S.C. Grierson C.S. Hirt H. Knight M.R OXI1 kinase is necessary for oxidative burst-mediated signaling in Arabidopsis.Nature. 2004; 427: 858-861Crossref PubMed Scopus (454) Google Scholar), and a defect in the OXI1 pathway negatively affects plant growth by the fungus, resembling a pathogenic interaction. Overall, the differences between Colletotrichum spp.- and P. indica-conferred disease resistance indicate that a number of different mechanisms exist that have yet to be elucidated. Further evidence exists that our present concepts of categorizing microbes as pathogenic or beneficial are inadequate. For example, F. culmorum was designated as pathogenic, as it can cause disease on a variety of crop plants. However, the F. culmorum isolate FcRed1 functions as a beneficial microbe and confers salt tolerance on its host dunegrass Leymus mollis, but isolates from non-coastal dunegrass do not have this property (Rodriguez et al., 2008Rodriguez R.J. Henson J. Van Volkenburgh E. Hoy M. Wright L. Beckwith F. Kim Y.O. Redman R.S Stress tolerance in plants via habitat-adapted symbiosis.ISME J. 2008; 2: 404-416Crossref PubMed Scopus (703) Google Scholar). C. protuberata is a plant pathogen for several monocots, but isolate Cp4666D confers heat and drought tolerance to its host plant D. lanuginosum (Rodriguez et al., 2008Rodriguez R.J. Henson J. Van Volkenburgh E. Hoy M. Wright L. Beckwith F. Kim Y.O. Redman R.S Stress tolerance in plants via habitat-adapted symbiosis.ISME J. 2008; 2: 404-416Crossref PubMed Scopus (703) Google Scholar). While Curvularia species are not known to have broad disease-host ranges, C. protuberata from the monocot D. lanuginosum also confers heat tolerance on tomato (Marquez et al., 2007Marquez L.M. Redman R.S. Rodriguez R.J. Roossinck M.J A virus in a fungus in a plant: three way symbiosis required for thermal tolerance.Science. 2007; 315: 513-515Crossref PubMed Scopus (590) Google Scholar; Rodriguez et al., 2008Rodriguez R.J. Henson J. Van Volkenburgh E. Hoy M. Wright L. Beckwith F. Kim Y.O. Redman R.S Stress tolerance in plants via habitat-adapted symbiosis.ISME J. 2008; 2: 404-416Crossref PubMed Scopus (703) Google Scholar). The ability of pathogenic Colletotrichum species to switch to a beneficiary lifestyle reveals that we still understand very little about the molecular basis of the plant–microbe interactions dictating friend–foe relationships. Some microbes can also be present in plants without showing disease symptoms. For example, Colletotrichum acutatum can colonize pepper, eggplant, bean, and tomato without causing disease but, with other plants, such as strawberry, disease symptoms become evident (Freeman et al., 2001Freeman S. Horowitz S. Sharon A Pathogenic and nonpathogenic lifestyles in Colletotrichum acutatum from strawberry and other plants.Phytopathol. 2001; 91: 986-992Crossref PubMed Scopus (126) Google Scholar). So it appears that a number of microbes have a host-dependent lifestyle as pathogenic or beneficiary partner of plants. It is important to point out that plant-associated microbial communities also include viruses and algae. Bacteria, fungi, viruses, and algae can all contribute to the outcome of the plant–microbial interaction and hence increase the complexity of studying these interactions. Moreover, fungi may also harbor bacteria and viruses which can affect the outcome of the plant–microbe interaction. For example, the Cp4666D isolate of C. protuberata, which was isolated from plants growing in geothermal soils, contains a double-stranded RNA virus that is required for conferring heat tolerance to its host plants (Marquez et al., 2007Marquez L.M. Redman R.S. Rodriguez R.J. Roossinck M.J A virus in a fungus in a plant: three way symbiosis required for thermal tolerance.Science. 2007; 315: 513-515Crossref PubMed Scopus (590) Google Scholar). In the absence of the virus, C. protuberata Cp4666D can still colonize its host, but has lost its ability to confer heat tolerance to the plants. Therefore, in this case, a ménage-a-trois (a virus in a fungus in a plant) is required for heat tolerance.