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The unseen rhizosphere root–soil–microbe interactions for crop production
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ScienceDirect The unseen rhizosphere root–soil–microbe interactions for crop production Ruifu Zhang1,2, Jorge M Vivanco3 and Qirong Shen1 The underground root–soil–microbe interactions are extremely complex, but vitally important for aboveground plant growth, health and fitness. The pressure to reduce our reliance on agrochemicals, and sustainable efforts to develop agriculture makes rhizosphere interactions’ research a hotspot. Recent advances provide new insights about the signals, pathways, functions and mechanisms of these interactions. In this review, we provide an overview about recent progress in rhizosphere interaction networks in crops. We also discuss a holistic view of the root–soil–rhizomicrobiome interactions achieved through the advances of omics and bioinformatics technologies, and the potential strategies to manage the complex rhizosphere interactions for enhancing crop production. Addresses 1 Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural University, Nanjing, 210095, PR China 2 Key Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, PR China 3 Department of Horticulture and Landscape Architecture and Center for Rhizosphere Biology, Colorado State University, Fort Collins, CO 80523, United States Corresponding author: Shen, Qirong ([email protected])
Current Opinion in Microbiology 2017, 37:8–14 This review comes from a themed issue on Environmental microbiology Edited by Marcio C Silva-Filho and Jorge Vivanco
http://dx.doi.org/10.1016/j.mib.2017.03.008 1369-5274/ã 2017 Elsevier Ltd. All rights reserved.
Introduction Increasing word population needs more crop production, and this has so far been achieved by the input of chemical fertilizers and pesticides. As the gateway for plants to uptake water and nutrients, and to interact with the soil, the plant rhizosphere can potentially be managed to increase crop yields while decreasing agrochemicals’ input. The rhizosphere, which is considered as the second genome of plants, is a hotspot for root–soil–microbe Current Opinion in Microbiology 2017, 37:8–14
interactions [1]. Roots secrete large amounts of fixed carbon as secretions, and they also deposit root cap border cells and polysaccharide mucilage [2–4]. Thus, the rhizosphere is a very attractive, nutrient-rich environment for microbes. In the rhizosphere, plant roots take up water and nutrients from soil and exert their effects on the adjacent soil through rhizodeposits. Rhizosphere microbes are actively involved in root–soil interactions, while the microbe– microbe and soil–microbe interactions in rhizosphere are also mediated by the roots [1]. More important, the direct root–microbe interactions play vital roles for plant growth, health and fitness. The intricate interactions in the rhizosphere indicate that all the partners (plant roots, soil and microbes) of the tripartite interactions can be manipulated or engineered to shift the direction in favor of plants for sustainable agricultural gains [5–7]. Rhizosphere engineering may ultimately reduce our reliance on agrochemicals by replacing their functions with beneficial microbes, but this strategy is largely based on the indepth understanding of rhizosphere root–soil–microbe interactions. Many insights have emerged from the model plant Arabidopsis [8], however, in recent years, rhizosphere studies have paid more attention to crops due to the urgent need to develop agriculture in a sustainable way. This review will introduce the recent progresses in rhizosphere of root–soil–microbe interactions (Figure 1), particularly of crops. Our discussion is mainly targeted to the plant beneficial microbes, while the soil borne pathogens are not the focus of this review.
Soil microbes are actively participating in the root–soil interactions The root–soil interface is a critical gateway for plants to take up water and nutrients from soils and exert their effects on soils through rhizodeposits. Under natural conditions, root–soil interactions are very complex with a multitude of microbes are actively participating in the association. Arbuscular mycorrhizal fungi (AMF) colonize more than 80% of terrestrial plants, and they help plant roots to uptake soil phosphorus. Some other rhizosphere microbes can fix nitrogen, release plant available phosphorus, potassium and other micronutrients, and assist the root in the efficient uptake of these nutrients [9]. The interaction between plants and soil, a belowground process termed as plant–soil feedback (PSF), is recognized as a major driver of plant community dynamics and nutrient www.sciencedirect.com
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Plant roots mediate microbe–microbe and soil–microbe interactions in the rhizosphere for their benefits
Figure 1
Soil
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Soil Current Opinion in Microbiology
Schematic representation of rhizosphere root–soil–microbe interactions. Soil microbes are actively involved in the root–soil interactions; Root mediate microbe–microbe and soil–microbe interactions in the rhizosphere; Direct root–microbe interactions involve extensive signal communications; Holistic view of the root– soil–rhizomicrobiome interactions.
cycling. A change in the composition of a plant community leads to a change in litter quality, which alters the local nutrient cycling process and soil conditions; the changed soil conditions may in turn drive a further change in plant community composition [10]. However, the plant-mediated PFS often neglects the roles of rootassociated microbes, which determines the decomposition rate of plant litter and directly or indirectly affect the plants. Recent studies have challenged the plant-centered view of PSF, suggesting mechanisms of microbialmediated PSF, and proposed the term plant–microbe–soil feedback (PMSF) [11,12]. The rhizosphere soil differs chemically and physically from bulk soil due to the effect of root exudates and other root deposits. However, it is argued that the direct influence of root exudates is limited, because the root exudates are rapidly assimilated by root-associated microbes, and are modified before released into the rhizosphere soil by the microbes themselves [13]. Indeed, recent studies with stable isotope-labeled root exudates demonstrate the fast assimilation and response of rhizosphere microbes to root exudates [14,15]. The assimilation of root deposits by rhizosphere microbes may improve soil quality, for example, it is reported that root polysaccharides induced the biofilm matrix production of plant-beneficial Bacillus subtilis, which resulted in the enhanced root colonization and plant beneficial effects [16], and the biofilm matrix in the rhizosphere may also help maintain the soil moisture and facilitate the formation of soil aggregation. www.sciencedirect.com
At the scale of meters or kilometers, environmental parameters have relatively large effect on the soil microbial communities, but in the microscale environments like the rhizosphere, microbial communities are likely to be dominated by the microbial interactions [17]. It has been reported that interactions of root-associated microbes are more complex than those of microbes in bulk soil probably due to the density and diversity of microbial cells in rhizosphere, and predominant interactions are positive (>80%), indicating that the rhizosphere has a greater potential for mutualistic associations [18]. Plant roots also mediate indirect interactions of plant beneficial and pathogenic microbes through the root secreted signals, which are usually for the benefits of plants themselves. Studies show that the attack of crops by soil borne pathogens is proceeded by the recruitment and stimulation of antagonistic bacteria by roots, which is a potential plant defense strategy against pathogen attack [1]. For example, in a split root system, the infection by the wilt disease pathogen Fusarium oxysporum f. sp. cucumerinum (FOC) increased the cucumber root secretion of citric acid and fumaric acid, which helped to recruit plant beneficial B. amyloliquefaciens SQR9 and enhanced its root colonization [19]. Infection of Pythium ultimum on one side of barley roots induced the expression of the 2,4-diacetylphloroglucinol (DAPG) biosynthesis gene phlA of the biocontrol bacterium Pseudomonas fluorescens CHA0 in another side of the roots. This induction was through increased secretion of vanillic acid, fumaric acid and pcoumaric acid, which could induce DAPG production of CHA0 in vitro at very low concentrations [20]. Plant roots have been shown to secrete components that interfere with quorum sensing (QS) [21,22], a cell–cell signaling mechanism in bacteria that is very important in group coordinated processes [23,24]. Many root-associated bacteria require QS for colonization of the rhizosphere and regulate a wide range of phenotypes including rhizosphere competence, virulence, conjugation, secretion of hydrolytic enzymes, and the production of secondary metabolites [25]. The rhizosphere is potentially favorable for QS signaling due to the high bacterial density and diversity [26]. Plant roots can produce QSsignal mimics or QS-interfering molecules and result in the quorum quenching (QQ) [27]. Some crops, including rice, soybean and tomato, were found to secrete compounds having AHL-mimicking activities [21,28,29]. AHL signal-mimicking compounds seem to be important in determining the outcome of interactions between plants and a diverse range of pathogenic microbes. QQ has been proposed as a novel biocontrol strategy against plant pathogens [27]. However, it is possible that QQ strategies may also prevent QS-regulated functions in plant beneficial bacteria [30]. Current Opinion in Microbiology 2017, 37:8–14
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Microorganisms play critical roles in soil formation from rocks and minerals, and together plant roots and soil microorganisms synergistically enhance rock weathering and soil maturation [31,32]. Recently, a new concept ‘mineralosphere’ was coined to describe the interface of the rocks (or mineral surfaces) and the surrounding soil with the associated microbial communities [33]. Plant roots exert strong effects on microbial-driven soil nutrient cycling. Nitrification and denitrification are pivotal microbial-driven soil processes related to the N loss from terrestrial ecosystems through NO3 leaching and gaseous N2 emission. The loss of ammonium fertilizer is mainly caused by nitrification and consequent denitrification, and these soil processes are critical for increasing the N-use efficiency (NUE) of crops [34]. Plant roots mediate these soil-microbe interaction processes through the secretion of biological nitrification inhibitors (BNIs) and biological denitrification inhibitors (BDIs) [35]. Recently, an efficient novel BNI, 1,9-decanediol, was identified in rice root exudates with the potential to be used in agriculture to improve NUE [36]. BNIs and BDIs can be exploited by breeding programs to develop crop cultivars with improved crop NUE and reduce N loss from the field, benefiting both the agricultural production and the environment. Another effect of roots on microbe–soil interactions is the rhizosphere priming effect (RPE). Labile organic substances released from roots accelerate the decomposition of soil organic matter (SOM) and stimulate the dissolution of insoluble minerals by rhizosphere microbes [4]. Studies in plant growth chambers and greenhouses indicate that the RPE varies widely, ranging from 17% to 380% enhancement of SOM turnover [37], and a recent meta-analysis showed that root-accelerated mineralization and priming could account for up to one-third of the total C and N mineralized in temperature forest soils, and these effects could be induced by relatively modest fluxes of the root-derived C [38]. The RPE can be significantly influenced by both plant traits and rhizosphere properties [39]. Although the quality and quantity of root exudates are thought to be key plant traits controlling RPE [40], however, the actual traits responsible for the large observed differences in RPE are virtually not clear [39]. A recent study indicated root biomass and length played a minor role in the plant species variation in RPE, while rhizosphere acidification caused by root exudates was shown to be an important factor affecting the magnitude and direction of RPE [41].
Direct root–microbe interactions involve extensive signal communications Rhizosphere is not only a battlefield of roots and soilborne pathogens, but also a playground for roots and beneficial microbes [42]. Due to the chemoattractant and signaling of root exudates and the biotic surface of the rhizoplane for attachment, roots are colonized or associated with Current Opinion in Microbiology 2017, 37:8–14
various microbes. These associations can be beneficial, harmful or neutral, and can significantly influence plant growth, health and fitness. Root secreted flavonoids, strigolactones, cutin monomers, phenolic acids, organic acids and volatiles have been recognized as signals to regulate root–microbe interactions and microbial gene expression [43]. It is very likely that many more chemical signals secreted by the root will be identified and potentially used to enhance the root colonization of beneficial microbes for crop production. A recent study, for example, showed that root secreted methyl salicylate could induce root colonization of beneficial Bacillus subtilis strain [44]. Rhizosphere beneficial microbes actively respond to root exudates by adjusting their transcriptional program toward traits involved in chemotaxis, mobility, biofilm formation, detoxification, transportation, polysaccharide degradation and secondary metabolism [45,46]. Once rhizosphere beneficial bacteria are established on the root, root exudates components may function as environmental cues to promote biofilm formation on the root surface [16]. Many excellent reviews have elegantly reviewed the mechanisms of root–microbe interactions, including their functions and the communication signals [8,47–50]. A recent study demonstrated interesting synergy of roots and associated bacterium for plant growth promotion; the plant beneficial Bacillus amyloliquefaciens SQR9 stimulated the secretion of tryptophan from roots, and then used tryptophan to produce the phytohormone auxin in the rhizosphere to promote plant growth [51]. Rhizosphere microorganisms do not only perceive plant root secreted signals, they also release diverse signaling molecules to influence their plant hosts for enhancing biotic and abiotic stress resistance or tolerance, root development and plant growth. Some PGPR strains release various molecules that serve as elicitors of plant induced systemic resistance (ISR), and these molecules include AHL-type QS molecules, diffusible signal factor diketopiperazines (DKPs), rhizosphere pseudomonadsproduced antibiotics (such as DAPG, pyocyanin), rhizosphere bacilli-produced lipopeptides and polyketides, siderophores, biosurfactants, and volatile organic chemicals (VOCs) (such as 2,3-butanediol and indole) [52–54]. Beneficial Bacillus subtilis GB03 emitted volatile 2,3butanediol, which was demonstrated to trigger induced systemic tolerance (IST) in plants through regulating the transcription of the high-affinity K+ transporter 1 (HKT1) in plant shoots and roots [55,56]. Rhizosphere microbes also release chemical molecules to affect plant root development. High concentration of these molecules inhibit primary root elongation and promote lateral root and root hair formation, indicating that these effects are through modulation of the endogenous root development programs. Some rhizosphere bacteria or fungi produce auxin, which directly interfere with root auxin signaling [57]. But, indole derivatives produced by root endophyte www.sciencedirect.com
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Piriformospora indica are not involved in root development and growth of barley, instead, they are required for biotrophic colonization of barley roots [58,59]. Other signals secreted by rhizosphere bacteria or fungi included AHLs [60–62], DKPs [63], the volatile compounds of indole [64] and dimethyl disulfide [65], the antibiotics DAPG [66] and pyocyanin [67]. These molecules interfered with the root auxin signaling pathways to modulate plant root architecture systems. The detailed regulating mechanism of endogenous root development pathways is not the scope of this review, and some excellent reviews are referred [68–70].
Holistic view of the root–soil–rhizomicrobiome interactions It is widely recognized that most of (>99%) the soil microorganisms are not yet cultured, but they may play important roles for plant productivity. With the development of culture-independent ‘omics’ and bioinformatics approaches, deeper insights into the structures and functions of crop rhizomicrobiomes provided holistic view of the root–soil–rhizomicrobiome interactions. The key questions are how is the rhizomicrobiome assembled and what factors shape its structure? Besides the model plant Arabidopsis [71–74], rhizomicrobiomes of many crops are also characterized, including rice [75], maize [76], wheat [77], barley [78] and soybean [79]. These studies confirmed that the rhizomicrobiome consist of a subset of the bulk soil microbiome. Soil type is identified as a major factor shaping the composition of the rhizomicrobiome. However, under identical environmental conditions and soils, the plant genotype is the main factor affecting the structure and function of the rhizomicrobiome, indicating that the plant acts as a filter for its own rhizomicrobiome. In natural ecosystems with long-term co-evolution of root and rhizomicrobiome, the effect of plant genotype is thought to be higher [80]. The plant genotype-mediated effects on rhizomicrobiome can have large effects on host growth and health [81]. Based on these well characterized rhizomicrobiomes of Arabidopsis and several crops, a two-step selection model [82] and later a three step enrichment model have been proposed to unveil the assembly process of the microbiome from bulk soil to the rhizosphere [83]. In both models, the bulk soil provides a microbial seed bank, the physical–chemical properties, the biogeography and climate conditions. In turn, the rhizosphere provides the rhizodeposits and other root factors such as oxygen and pH [84], the plant genotype and developmental stage, and plant defense-related hormones [85]. Specific microbial traits like biofilm formation and surface adhesion may also determine who can colonize these root compartments. Therefore, the structure of the rhizomicrobiome is the result of complex root–soil–microbe interactions.
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Concluding remarks Despite great advances in understanding the complex networks in the rhizosphere, our understanding is still in its infancy, and most of our insights are derived from model plants with the study for major crops just starting. The complexity of rhizosphere continues to present a multitude of ‘black boxes’ to our understanding of fundamental issues concerning signals, recognition and pathways, cost and balance, function and management of root–soil–microbe interactions. With more restrictive regulations for the use of agrochemicals being implemented and the demand for more food to feed the ever-increasing world population, comprehensive studies of the rhizosphere interactions to support crop production are even more urgent. The close interactions between crops and rhizosphere microbes (and other plant microbiomes) have catalyzed the view of plants as a superorganism-the holobiont [86]. Any modification of a component of the holobiont may affect other modules; thus application of beneficial microbes or any agricultural practice to enhance the rhizosphere microbial activity should take into account the other components. For rhizosphere management, all the components (plant roots, soil and microbes) can be manipulated or engineered to favor crop growth and health. The current practices, such as the application of biofertilizers and biocontrol agents, or soil amendments with organic materials, are mainly targeting the microbes and soils, while the crops as hosts are usually neglected. Enhancing root-beneficial microbe associations through crop breeding should be undertaken [87]. Unfortunately, the domestication and the breeding of modern crop cultivars have affected the associated microbiome; for instance, mycorrhizal colonization of modern crop cultivars is lower than that of ancestral lines or wild-type plants, possibly due to the highly fertile soil conditions needed by modern cultivars [87]. Discovery of novel rhizosphere signaling compounds, elucidation of the mechanisms involved in the perception of the molecular dialog between plant roots and the rhizomicrobiome, identification of crop key genes controlling beneficial microbes’ root colonization are important issues for crop breeding to take into account.
Acknowledgements We acknowledge the journal of Current Opinion in Microbiology for inviting us to write this review. The authors also thank Dr. Yunpeng Liu for help with the figure. R. Z. and Q. S. are supported by the National Key Basic Research Program of China (973 program, 2015CB150505), National Natural Science Foundation of China (31330069, 31572214) and the 111 Project (B12009).
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56. Zhang H, Kim M, Sun Y, Dowd SE, Shi H, Pare´ PW: Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol. Plant Microbe Interact. 2008, 21:737-744. 57. Spaepen S, Bossuyt S, Engelen K, Marchal K, Vanderleyden J: Phenotypical and molecular responses of Arabidopsis thaliana roots as a result of inoculation with the auxinproducing bacterium Azospirillum brasilense. New Phytol. 2014, 201:850-861. 58. Lee YC, Johnson JM, Chien CT, Sun C, Cai D, Lou B, Oelmu¨ller R, Yeh KW: Growth promotion of Chinese cabbage and Arabidopsis by Piriformospora indica is not stimulated by mycelium-synthesized auxin. Mol. Plant Microbe Interact. 2011, 24:421-431. 59. Hilbert M, Voll LM, Ding Y, Hofmann J, Sharma M, Zuccaro A: Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots. New Phytol. 2012, 196:520-534. 60. Ortı´z-Castro R, Martı´nez-Trujillo M, Lo´pez-Bucio J: N-Acyl-Lhomoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ. 2008, 31:1497-1509. 61. Liu F, Bian Z, Jia Z, Zhao Q, Song S: The GCR1 and GPA1 participate in promotion of Arabidopsis primary root elongation induced by N-acyl-homo-serine lactones, the bacterial quorum-sensing signals. Mol. Plant Microbe Interact. 2012, 25:677-683. 62. Zhao Q, Zhang C, Jia Z, Huang Y, Li H, Song S: Involvement of calmodulin in regulation of primary root elongation by N-3oxo-hexanoyl homoserine lactone in Arabidopsis thaliana. Front. Plant Sci. 2015, 5:807. 63. Ortiz-Castro R, Dı´az-Pe´rez C, Martı´nez-Trujillo M, del Rı´o RE, Campos-Garcı´a J, Lo´pez-Bucio J: Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:7253-7258. 64. Bailly A, Groenhagen U, Schulz S, Geisler M, Eberl L, Weisskopf L: The inter-kingdom volatile signal indole promotes root development by interfering with auxin signalling. Plant J. 2014, 80:758-771. 65. Meldau DG, Meldau S, Hoang LH, Underberg S, Wu¨nsche H, Baldwin IT: Dimethyl disulfide produced by the naturally associated bacterium Bacillus sp B55 promotes Nicotiana attenuata growth by enhancing sulfur nutrition. Plant Cell 2013, 25:2731-2747. 66. Brazelton JN, Pfeufer EE, Sweat TA, Gardener BB, Coenen C: 2,4diacetylphloroglucinol alters plant root development. Mol. Plant Microbe Interact. 2008, 21:1349-1358. 67. Ortiz-Castro R, Pelagio-Flores R, Me´ndez-Bravo A, RuizHerrera LF, Campos-Garcı´a J, Lo´pez-Bucio J: Pyocyanin, a virulence factor produced by Pseudomonas aeruginosa, alters root development through reactive oxygen species and ethylene signaling in Arabidopsis. Mol. Plant Microbe Interact. 2014, 27:364-378. Current Opinion in Microbiology 2017, 37:8–14
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68. Verbon EH, Liberman LM: Beneficial microbes affect endogenous mechanisms controlling root development. Trends Plant Sci. 2016, 21:218-229. 69. Contreras-Cornejo HA, Macias-Rodriguez L, Cortes-Penagos C, Lopez-Bucio J: Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol. 2009, 149:1579-1592. 70. Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CMJ: Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol. 2013, 162:304-318. 71. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG et al.: Defining the core Arabidopsis thaliana root microbiome. Nature 2012, 488:86-90. 72. Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E et al.: Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 2012, 488:91-95. 73. Schlaeppi K, Dombrowski N, Oter RG, Ver Loren van Themaat E, Schulze-Lefert P: Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:585-592. 74. Bai Y, Mu¨ller DB, Srinivas G, Garrido-Oter R, Potthoff E, Rott M, Dombrowski N, Mu¨nch PC, Spaepen S, Remus-Emsermann M et al.: Functional overlap of the Arabidopsis leaf and root microbiota. Nature 2015, 528:364-369. 75. Edwards J, Johnson C, Santos-Medellı´n C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V: Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:E911-E920. A very detailed characterization of the root-associated microbiomes of the major crop by deep sequencing, using rice plants grown under controlled conditions as well as field cultivation at multiple sites. 76. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE: Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:6548-6553. 77. Ofek-Lalzar M, Sela N, Goldman-Voronov M, Green SJ, Hadar Y, Minz D: Niche and host-associated functional signatures of the root surface microbiome. Nat. Commun. 2014, 5:4950.
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78. Bulgarelli D, Garrido-Oter R, Mu¨nch PC, Weiman A, Dro¨ge J, Pan Y, McHardy AC, Schulze-Lefert P: Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 2015, 17:392-403. 79. Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM: Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J. 2014, 8:1577-1587. 80. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH: Going back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 2013, 11:789-799. 81. Haney CH, Samuel BS, Bush J, Ausubel FM: Associations with rhizosphere bacteria can confer an adaptive advantage to plants. Nat. Plants 2015, 1:15051. This study demonstrated that the small plant genotype-mediated effects on rhizomicrobiome can have large effects on host growth and health. 82. Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E, Schulze-Lefert P: Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 2013, 64:807-838. 83. Reinhold-Hurek B, Bu¨nger W, Burbano CS, Sabale M, Hurek T: Roots shaping their microbiome: global hotspots for microbial activity. Annu. Rev. Phytopathol. 2015, 53:403-424. 84. Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM: Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic related compounds predominantly modulate the soil microbiome. J. Biol. Chem. 2013, 288:4502-4512. 85. Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J, McDonald M, Malfatti S, Glavina del Rio T, Jones CD, Tringe SG et al.: Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 2015, 349:860864. This study demonstrated that plant immune signal, salicylic acid, modulates colonization of the root by specific bacterial families, and drove the selection from the available microbial communities to sculpt the root microbiome. 86. Pieterse CM, de Jonge R, Berendsen RL: The soil-borne supremacy. Trends Plant Sci. 2016, 21:171-173. 87. Germida JJ, Siciliano SD: Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivars. Biol. Fertil. Soils 2001, 33:410-415.
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ScienceDirect The unseen rhizosphere root–soil–microbe interactions for crop production Ruifu Zhang1,2, Jorge M Vivanco3 and Qirong Shen1 The underground root–soil–microbe interactions are extremely complex, but vitally important for aboveground plant growth, health and fitness. The pressure to reduce our reliance on agrochemicals, and sustainable efforts to develop agriculture makes rhizosphere interactions’ research a hotspot. Recent advances provide new insights about the signals, pathways, functions and mechanisms of these interactions. In this review, we provide an overview about recent progress in rhizosphere interaction networks in crops. We also discuss a holistic view of the root–soil–rhizomicrobiome interactions achieved through the advances of omics and bioinformatics technologies, and the potential strategies to manage the complex rhizosphere interactions for enhancing crop production. Addresses 1 Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural University, Nanjing, 210095, PR China 2 Key Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, PR China 3 Department of Horticulture and Landscape Architecture and Center for Rhizosphere Biology, Colorado State University, Fort Collins, CO 80523, United States Corresponding author: Shen, Qirong ([email protected])
Current Opinion in Microbiology 2017, 37:8–14 This review comes from a themed issue on Environmental microbiology Edited by Marcio C Silva-Filho and Jorge Vivanco
http://dx.doi.org/10.1016/j.mib.2017.03.008 1369-5274/ã 2017 Elsevier Ltd. All rights reserved.
Introduction Increasing word population needs more crop production, and this has so far been achieved by the input of chemical fertilizers and pesticides. As the gateway for plants to uptake water and nutrients, and to interact with the soil, the plant rhizosphere can potentially be managed to increase crop yields while decreasing agrochemicals’ input. The rhizosphere, which is considered as the second genome of plants, is a hotspot for root–soil–microbe Current Opinion in Microbiology 2017, 37:8–14
interactions [1]. Roots secrete large amounts of fixed carbon as secretions, and they also deposit root cap border cells and polysaccharide mucilage [2–4]. Thus, the rhizosphere is a very attractive, nutrient-rich environment for microbes. In the rhizosphere, plant roots take up water and nutrients from soil and exert their effects on the adjacent soil through rhizodeposits. Rhizosphere microbes are actively involved in root–soil interactions, while the microbe– microbe and soil–microbe interactions in rhizosphere are also mediated by the roots [1]. More important, the direct root–microbe interactions play vital roles for plant growth, health and fitness. The intricate interactions in the rhizosphere indicate that all the partners (plant roots, soil and microbes) of the tripartite interactions can be manipulated or engineered to shift the direction in favor of plants for sustainable agricultural gains [5–7]. Rhizosphere engineering may ultimately reduce our reliance on agrochemicals by replacing their functions with beneficial microbes, but this strategy is largely based on the indepth understanding of rhizosphere root–soil–microbe interactions. Many insights have emerged from the model plant Arabidopsis [8], however, in recent years, rhizosphere studies have paid more attention to crops due to the urgent need to develop agriculture in a sustainable way. This review will introduce the recent progresses in rhizosphere of root–soil–microbe interactions (Figure 1), particularly of crops. Our discussion is mainly targeted to the plant beneficial microbes, while the soil borne pathogens are not the focus of this review.
Soil microbes are actively participating in the root–soil interactions The root–soil interface is a critical gateway for plants to take up water and nutrients from soils and exert their effects on soils through rhizodeposits. Under natural conditions, root–soil interactions are very complex with a multitude of microbes are actively participating in the association. Arbuscular mycorrhizal fungi (AMF) colonize more than 80% of terrestrial plants, and they help plant roots to uptake soil phosphorus. Some other rhizosphere microbes can fix nitrogen, release plant available phosphorus, potassium and other micronutrients, and assist the root in the efficient uptake of these nutrients [9]. The interaction between plants and soil, a belowground process termed as plant–soil feedback (PSF), is recognized as a major driver of plant community dynamics and nutrient www.sciencedirect.com
Rhizosphere root–soil–microbe interactions Zhang, Vivanco and Shen 9
Plant roots mediate microbe–microbe and soil–microbe interactions in the rhizosphere for their benefits
Figure 1
Soil
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Soil Current Opinion in Microbiology
Schematic representation of rhizosphere root–soil–microbe interactions. Soil microbes are actively involved in the root–soil interactions; Root mediate microbe–microbe and soil–microbe interactions in the rhizosphere; Direct root–microbe interactions involve extensive signal communications; Holistic view of the root– soil–rhizomicrobiome interactions.
cycling. A change in the composition of a plant community leads to a change in litter quality, which alters the local nutrient cycling process and soil conditions; the changed soil conditions may in turn drive a further change in plant community composition [10]. However, the plant-mediated PFS often neglects the roles of rootassociated microbes, which determines the decomposition rate of plant litter and directly or indirectly affect the plants. Recent studies have challenged the plant-centered view of PSF, suggesting mechanisms of microbialmediated PSF, and proposed the term plant–microbe–soil feedback (PMSF) [11,12]. The rhizosphere soil differs chemically and physically from bulk soil due to the effect of root exudates and other root deposits. However, it is argued that the direct influence of root exudates is limited, because the root exudates are rapidly assimilated by root-associated microbes, and are modified before released into the rhizosphere soil by the microbes themselves [13]. Indeed, recent studies with stable isotope-labeled root exudates demonstrate the fast assimilation and response of rhizosphere microbes to root exudates [14,15]. The assimilation of root deposits by rhizosphere microbes may improve soil quality, for example, it is reported that root polysaccharides induced the biofilm matrix production of plant-beneficial Bacillus subtilis, which resulted in the enhanced root colonization and plant beneficial effects [16], and the biofilm matrix in the rhizosphere may also help maintain the soil moisture and facilitate the formation of soil aggregation. www.sciencedirect.com
At the scale of meters or kilometers, environmental parameters have relatively large effect on the soil microbial communities, but in the microscale environments like the rhizosphere, microbial communities are likely to be dominated by the microbial interactions [17]. It has been reported that interactions of root-associated microbes are more complex than those of microbes in bulk soil probably due to the density and diversity of microbial cells in rhizosphere, and predominant interactions are positive (>80%), indicating that the rhizosphere has a greater potential for mutualistic associations [18]. Plant roots also mediate indirect interactions of plant beneficial and pathogenic microbes through the root secreted signals, which are usually for the benefits of plants themselves. Studies show that the attack of crops by soil borne pathogens is proceeded by the recruitment and stimulation of antagonistic bacteria by roots, which is a potential plant defense strategy against pathogen attack [1]. For example, in a split root system, the infection by the wilt disease pathogen Fusarium oxysporum f. sp. cucumerinum (FOC) increased the cucumber root secretion of citric acid and fumaric acid, which helped to recruit plant beneficial B. amyloliquefaciens SQR9 and enhanced its root colonization [19]. Infection of Pythium ultimum on one side of barley roots induced the expression of the 2,4-diacetylphloroglucinol (DAPG) biosynthesis gene phlA of the biocontrol bacterium Pseudomonas fluorescens CHA0 in another side of the roots. This induction was through increased secretion of vanillic acid, fumaric acid and pcoumaric acid, which could induce DAPG production of CHA0 in vitro at very low concentrations [20]. Plant roots have been shown to secrete components that interfere with quorum sensing (QS) [21,22], a cell–cell signaling mechanism in bacteria that is very important in group coordinated processes [23,24]. Many root-associated bacteria require QS for colonization of the rhizosphere and regulate a wide range of phenotypes including rhizosphere competence, virulence, conjugation, secretion of hydrolytic enzymes, and the production of secondary metabolites [25]. The rhizosphere is potentially favorable for QS signaling due to the high bacterial density and diversity [26]. Plant roots can produce QSsignal mimics or QS-interfering molecules and result in the quorum quenching (QQ) [27]. Some crops, including rice, soybean and tomato, were found to secrete compounds having AHL-mimicking activities [21,28,29]. AHL signal-mimicking compounds seem to be important in determining the outcome of interactions between plants and a diverse range of pathogenic microbes. QQ has been proposed as a novel biocontrol strategy against plant pathogens [27]. However, it is possible that QQ strategies may also prevent QS-regulated functions in plant beneficial bacteria [30]. Current Opinion in Microbiology 2017, 37:8–14
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Microorganisms play critical roles in soil formation from rocks and minerals, and together plant roots and soil microorganisms synergistically enhance rock weathering and soil maturation [31,32]. Recently, a new concept ‘mineralosphere’ was coined to describe the interface of the rocks (or mineral surfaces) and the surrounding soil with the associated microbial communities [33]. Plant roots exert strong effects on microbial-driven soil nutrient cycling. Nitrification and denitrification are pivotal microbial-driven soil processes related to the N loss from terrestrial ecosystems through NO3 leaching and gaseous N2 emission. The loss of ammonium fertilizer is mainly caused by nitrification and consequent denitrification, and these soil processes are critical for increasing the N-use efficiency (NUE) of crops [34]. Plant roots mediate these soil-microbe interaction processes through the secretion of biological nitrification inhibitors (BNIs) and biological denitrification inhibitors (BDIs) [35]. Recently, an efficient novel BNI, 1,9-decanediol, was identified in rice root exudates with the potential to be used in agriculture to improve NUE [36]. BNIs and BDIs can be exploited by breeding programs to develop crop cultivars with improved crop NUE and reduce N loss from the field, benefiting both the agricultural production and the environment. Another effect of roots on microbe–soil interactions is the rhizosphere priming effect (RPE). Labile organic substances released from roots accelerate the decomposition of soil organic matter (SOM) and stimulate the dissolution of insoluble minerals by rhizosphere microbes [4]. Studies in plant growth chambers and greenhouses indicate that the RPE varies widely, ranging from 17% to 380% enhancement of SOM turnover [37], and a recent meta-analysis showed that root-accelerated mineralization and priming could account for up to one-third of the total C and N mineralized in temperature forest soils, and these effects could be induced by relatively modest fluxes of the root-derived C [38]. The RPE can be significantly influenced by both plant traits and rhizosphere properties [39]. Although the quality and quantity of root exudates are thought to be key plant traits controlling RPE [40], however, the actual traits responsible for the large observed differences in RPE are virtually not clear [39]. A recent study indicated root biomass and length played a minor role in the plant species variation in RPE, while rhizosphere acidification caused by root exudates was shown to be an important factor affecting the magnitude and direction of RPE [41].
Direct root–microbe interactions involve extensive signal communications Rhizosphere is not only a battlefield of roots and soilborne pathogens, but also a playground for roots and beneficial microbes [42]. Due to the chemoattractant and signaling of root exudates and the biotic surface of the rhizoplane for attachment, roots are colonized or associated with Current Opinion in Microbiology 2017, 37:8–14
various microbes. These associations can be beneficial, harmful or neutral, and can significantly influence plant growth, health and fitness. Root secreted flavonoids, strigolactones, cutin monomers, phenolic acids, organic acids and volatiles have been recognized as signals to regulate root–microbe interactions and microbial gene expression [43]. It is very likely that many more chemical signals secreted by the root will be identified and potentially used to enhance the root colonization of beneficial microbes for crop production. A recent study, for example, showed that root secreted methyl salicylate could induce root colonization of beneficial Bacillus subtilis strain [44]. Rhizosphere beneficial microbes actively respond to root exudates by adjusting their transcriptional program toward traits involved in chemotaxis, mobility, biofilm formation, detoxification, transportation, polysaccharide degradation and secondary metabolism [45,46]. Once rhizosphere beneficial bacteria are established on the root, root exudates components may function as environmental cues to promote biofilm formation on the root surface [16]. Many excellent reviews have elegantly reviewed the mechanisms of root–microbe interactions, including their functions and the communication signals [8,47–50]. A recent study demonstrated interesting synergy of roots and associated bacterium for plant growth promotion; the plant beneficial Bacillus amyloliquefaciens SQR9 stimulated the secretion of tryptophan from roots, and then used tryptophan to produce the phytohormone auxin in the rhizosphere to promote plant growth [51]. Rhizosphere microorganisms do not only perceive plant root secreted signals, they also release diverse signaling molecules to influence their plant hosts for enhancing biotic and abiotic stress resistance or tolerance, root development and plant growth. Some PGPR strains release various molecules that serve as elicitors of plant induced systemic resistance (ISR), and these molecules include AHL-type QS molecules, diffusible signal factor diketopiperazines (DKPs), rhizosphere pseudomonadsproduced antibiotics (such as DAPG, pyocyanin), rhizosphere bacilli-produced lipopeptides and polyketides, siderophores, biosurfactants, and volatile organic chemicals (VOCs) (such as 2,3-butanediol and indole) [52–54]. Beneficial Bacillus subtilis GB03 emitted volatile 2,3butanediol, which was demonstrated to trigger induced systemic tolerance (IST) in plants through regulating the transcription of the high-affinity K+ transporter 1 (HKT1) in plant shoots and roots [55,56]. Rhizosphere microbes also release chemical molecules to affect plant root development. High concentration of these molecules inhibit primary root elongation and promote lateral root and root hair formation, indicating that these effects are through modulation of the endogenous root development programs. Some rhizosphere bacteria or fungi produce auxin, which directly interfere with root auxin signaling [57]. But, indole derivatives produced by root endophyte www.sciencedirect.com
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Piriformospora indica are not involved in root development and growth of barley, instead, they are required for biotrophic colonization of barley roots [58,59]. Other signals secreted by rhizosphere bacteria or fungi included AHLs [60–62], DKPs [63], the volatile compounds of indole [64] and dimethyl disulfide [65], the antibiotics DAPG [66] and pyocyanin [67]. These molecules interfered with the root auxin signaling pathways to modulate plant root architecture systems. The detailed regulating mechanism of endogenous root development pathways is not the scope of this review, and some excellent reviews are referred [68–70].
Holistic view of the root–soil–rhizomicrobiome interactions It is widely recognized that most of (>99%) the soil microorganisms are not yet cultured, but they may play important roles for plant productivity. With the development of culture-independent ‘omics’ and bioinformatics approaches, deeper insights into the structures and functions of crop rhizomicrobiomes provided holistic view of the root–soil–rhizomicrobiome interactions. The key questions are how is the rhizomicrobiome assembled and what factors shape its structure? Besides the model plant Arabidopsis [71–74], rhizomicrobiomes of many crops are also characterized, including rice [75], maize [76], wheat [77], barley [78] and soybean [79]. These studies confirmed that the rhizomicrobiome consist of a subset of the bulk soil microbiome. Soil type is identified as a major factor shaping the composition of the rhizomicrobiome. However, under identical environmental conditions and soils, the plant genotype is the main factor affecting the structure and function of the rhizomicrobiome, indicating that the plant acts as a filter for its own rhizomicrobiome. In natural ecosystems with long-term co-evolution of root and rhizomicrobiome, the effect of plant genotype is thought to be higher [80]. The plant genotype-mediated effects on rhizomicrobiome can have large effects on host growth and health [81]. Based on these well characterized rhizomicrobiomes of Arabidopsis and several crops, a two-step selection model [82] and later a three step enrichment model have been proposed to unveil the assembly process of the microbiome from bulk soil to the rhizosphere [83]. In both models, the bulk soil provides a microbial seed bank, the physical–chemical properties, the biogeography and climate conditions. In turn, the rhizosphere provides the rhizodeposits and other root factors such as oxygen and pH [84], the plant genotype and developmental stage, and plant defense-related hormones [85]. Specific microbial traits like biofilm formation and surface adhesion may also determine who can colonize these root compartments. Therefore, the structure of the rhizomicrobiome is the result of complex root–soil–microbe interactions.
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Concluding remarks Despite great advances in understanding the complex networks in the rhizosphere, our understanding is still in its infancy, and most of our insights are derived from model plants with the study for major crops just starting. The complexity of rhizosphere continues to present a multitude of ‘black boxes’ to our understanding of fundamental issues concerning signals, recognition and pathways, cost and balance, function and management of root–soil–microbe interactions. With more restrictive regulations for the use of agrochemicals being implemented and the demand for more food to feed the ever-increasing world population, comprehensive studies of the rhizosphere interactions to support crop production are even more urgent. The close interactions between crops and rhizosphere microbes (and other plant microbiomes) have catalyzed the view of plants as a superorganism-the holobiont [86]. Any modification of a component of the holobiont may affect other modules; thus application of beneficial microbes or any agricultural practice to enhance the rhizosphere microbial activity should take into account the other components. For rhizosphere management, all the components (plant roots, soil and microbes) can be manipulated or engineered to favor crop growth and health. The current practices, such as the application of biofertilizers and biocontrol agents, or soil amendments with organic materials, are mainly targeting the microbes and soils, while the crops as hosts are usually neglected. Enhancing root-beneficial microbe associations through crop breeding should be undertaken [87]. Unfortunately, the domestication and the breeding of modern crop cultivars have affected the associated microbiome; for instance, mycorrhizal colonization of modern crop cultivars is lower than that of ancestral lines or wild-type plants, possibly due to the highly fertile soil conditions needed by modern cultivars [87]. Discovery of novel rhizosphere signaling compounds, elucidation of the mechanisms involved in the perception of the molecular dialog between plant roots and the rhizomicrobiome, identification of crop key genes controlling beneficial microbes’ root colonization are important issues for crop breeding to take into account.
Acknowledgements We acknowledge the journal of Current Opinion in Microbiology for inviting us to write this review. The authors also thank Dr. Yunpeng Liu for help with the figure. R. Z. and Q. S. are supported by the National Key Basic Research Program of China (973 program, 2015CB150505), National Natural Science Foundation of China (31330069, 31572214) and the 111 Project (B12009).
References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest
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Rhizosphere root–soil–microbe interactions Zhang, Vivanco and Shen 13
decanediol, was identified. Plant N-use efficiency (NUE) using15N-labeling method showed both BNI abilities and 1,9-decanediol amounts of root exudates were positively correlated with plant ammonium-use efficiency. This manuscript provided important new insights into the plant–bacterial interactions involved in the soil N cycle, and improved our understanding of the BNI capacity of rice in the context of NUE.
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