Communication in the Phytobiome
2017; Cell Press; Volume: 169; Issue: 4 Linguagem: Inglês
10.1016/j.cell.2017.04.025
ISSN1097-4172
AutoresJan E. Leach, Lindsay R. Triplett, Cristiana T. Argueso, Pankaj Trivedi,
Tópico(s)Plant tissue culture and regeneration
ResumoThe phytobiome is composed of plants, their environment, and diverse interacting microscopic and macroscopic organisms, which together influence plant health and productivity. These organisms form complex networks that are established and regulated through nutrient cycling, competition, antagonism, and chemical communication mediated by a diverse array of signaling molecules. Integration of knowledge of signaling mechanisms with that of phytobiome members and their networks will lead to a new understanding of the fate and significance of these signals at the ecosystem level. Such an understanding could lead to new biological, chemical, and breeding strategies to improve crop health and productivity. The phytobiome is composed of plants, their environment, and diverse interacting microscopic and macroscopic organisms, which together influence plant health and productivity. These organisms form complex networks that are established and regulated through nutrient cycling, competition, antagonism, and chemical communication mediated by a diverse array of signaling molecules. Integration of knowledge of signaling mechanisms with that of phytobiome members and their networks will lead to a new understanding of the fate and significance of these signals at the ecosystem level. Such an understanding could lead to new biological, chemical, and breeding strategies to improve crop health and productivity. The ecosystems within and surrounding plants, called phytobiomes, are teeming with microorganisms and macroorganisms. They include representatives from diverse taxa: viruses, bacteria, archaea, fungi, oomycetes, other plants, and animals. The biological interactions among these organisms encompass the full range encountered in any complex ecosystem, from competition, predation, and pathogenesis to mutualism and symbiosis. Interactions are influenced by environmental factors, including soil composition, temperature, humidity, irradiation, and wind. Teasing apart these intricate exchanges for applicable insight is an ongoing challenge, but one that could yield new intervention points for managing crop health. Understanding, and eventually directing, the functions of phytobiomes will require embracing their complexity. Plants and associated organisms influence one another through cycling of nutrients, chemical antagonism, or direct predation and feeding. Interactions are established and regulated, and sometimes inhibited, through the production and perception of physical and chemical cues. We focus this brief Review on the chemical languages mediating communication in the phytobiome, and how these signals are perceived and manipulated to affect plant performance. The first stage toward resolving phytobiome function has been exploration of the composition, distribution, and abundance of organisms within plant-associated communities. Plants associate with billions of organisms in millions of species, from viruses to arthropods, whose gene repertoires far surpass those of plants themselves (Table 1; see references). Metataxonomic approaches are high-throughput processes used to characterize the entire microbiota and allow comparisons of relationships among microbiome members (Marchesi and Ravel, 2015Marchesi J.R. Ravel J. The vocabulary of microbiome research: a proposal.Microbiome. 2015; 3: 31Crossref PubMed Google Scholar). Such approaches targeting bacterial and fungal composition have shown that genotype, environment, and plant compartment (i.e., spermosphere, endosphere, rhizosphere, phyllosphere) all influence community composition to varying degrees (Figure 1; [Hacquard et al., 2015Hacquard S. Garrido-Oter R. González A. Spaepen S. Ackermann G. Lebeis S. McHardy A.C. Dangl J.L. Knight R. Ley R. Schulze-Lefert P. Microbiota and host nutrition across plant and animal kingdoms.Cell Host Microbe. 2015; 17: 603-616Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar]). The plant aerial surface, or phyllosphere, which experiences fluctuations in nutrient availability and environmental conditions, harbors a more distinct microbiome compared with the more environmentally stable rhizosphere (zone of soil that is directly influenced by the plant root) (Remus-Emsermann et al., 2012Remus-Emsermann M.N. Tecon R. Kowalchuk G.A. Leveau J.H. Variation in local carrying capacity and the individual fate of bacterial colonizers in the phyllosphere.ISME J. 2012; 6: 756-765Crossref PubMed Scopus (29) Google Scholar). Whole-metagenome sequencing (WMS) studies, which offer a more comprehensive view of nonbacterial organisms, have determined that bacteria dominate all plant compartments and that bacterial diversity and density are highest in the rhizoplane (external root surface) (Hacquard et al., 2015Hacquard S. Garrido-Oter R. González A. Spaepen S. Ackermann G. Lebeis S. McHardy A.C. Dangl J.L. Knight R. Ley R. Schulze-Lefert P. Microbiota and host nutrition across plant and animal kingdoms.Cell Host Microbe. 2015; 17: 603-616Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar). The finding that plant genotype and plant niche can drive community composition has important implications for crop-improvement programs.Table 1Estimated Abundance, Diversity, and Number of Genes of Phytobiome Community Members from Published LiteratureGroupBelowgroundAbovegroundAbundance∗Diversity∗∗No. of genes∗∗∗Abundance∗Diversity∗∗No. of genes∗∗∗Bacteria (g−1 sample)106–1012∗102–106‡1012102–107∗101–105 ‡108Fungi (g−1 sample)103–108∗101–103‡1010101–103∗101–102‡106Archaea (g−1 sample)105–106∗101–102‡109101–102∗1–10‡105Virus (g−1 sample)106–109∗∗101–102‡‡109102–103∗∗1–50‡‡‡105Nematodes (g−1)101–102∗∗∗10°–101‡‡‡‡106Protists (g−1)105–106∗∗∗102–103‡‡‡1010Algae (g−1)103–106∗∗∗101–102‡‡‡‡‡109Arthropods (m−2)102–105∗∗∗101–103‡‡‡‡‡108Earthworms101–103 m−2∗∗∗10–15 ha−1‡‡‡‡‡106 m−2Belowground represents soil, root, and rhizosphere regions, while aboveground represents the phyllosphere. Units can vary strongly between taxonomic groups, depending on the method of analysis, data representation, and sample collection. Numbers are indicative only, as the majority of the soil biodiversity is yet to be explored, and because most estimates are based on single ecosystems or regions. Approximate number of genes per sample−1 were calculated based on the average number of genes in the members of representative groups X average abundance. For bacteria, fungi, virus, and archaea, data on gene copies were collected from IMG-JGI.∗ Gene copy numbers; ∗∗ virus like particles (VLPs); ∗∗∗ number of individuals‡Operational taxonomic units (OTUs); ‡‡ Unique VLPs; ‡‡‡ Unique sequences; ‡‡‡‡ genera; ‡‡‡‡‡ speciesBacteria: ∗ gene copy numbers g−1 samples: Belowground: (Rousk et al., 2010Rousk J. Bååth E. Brookes P.C. Lauber C.L. Lozupone C. Caporaso J.G. Knight R. Fierer N. Soil bacterial and fungal communities across a pH gradient in an arable soil.ISME J. 2010; 4: 1340-1351Crossref PubMed Scopus (0) Google Scholar, Siles and Margesin, 2016Siles J.A. Margesin R. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors?.Microb. Ecol. 2016; 72: 207-220Crossref PubMed Scopus (6) Google Scholar, Trivedi et al., 2016Trivedi P. Delgado-Baquerizo M. Trivedi C. Hu H. Anderson I.C. Jeffries T.C. Zhou J. Singh B.K. Microbial regulation of the soil carbon cycle: evidence from gene-enzyme relationships.ISME J. 2016; 10: 2593-2604Crossref PubMed Scopus (6) Google Scholar); Aboveground: (Williams and Marco, 2014Williams T.R. Marco M.L. Phyllosphere microbiota composition and microbial community transplantation on lettuce plants grown indoors.MBio. 2014; 5 (e01564–14)Crossref Scopus (14) Google Scholar). ‡ Operational taxonomic units (OTUs): Belowground: (Maestre et al., 2015Maestre F.T. Delgado-Baquerizo M. Jeffries T.C. Eldridge D.J. Ochoa V. Gozalo B. Quero J.L. García-Gómez M. Gallardo A. Ulrich W. et al.Increasing aridity reduces soil microbial diversity and abundance in global drylands.Proc. Natl. Acad. Sci. USA. 2015; 112: 15684-15689PubMed Google Scholar, Siles and Margesin, 2016Siles J.A. Margesin R. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors?.Microb. Ecol. 2016; 72: 207-220Crossref PubMed Scopus (6) Google Scholar, Trivedi et al., 2016Trivedi P. Delgado-Baquerizo M. Trivedi C. Hu H. Anderson I.C. Jeffries T.C. Zhou J. Singh B.K. Microbial regulation of the soil carbon cycle: evidence from gene-enzyme relationships.ISME J. 2016; 10: 2593-2604Crossref PubMed Scopus (6) Google Scholar); Aboveground: (Coleman-Derr et al., 2016Coleman-Derr D. Desgarennes D. Fonseca-Garcia C. Gross S. Clingenpeel S. Woyke T. North G. Visel A. Partida-Martinez L.P. Tringe S.G. Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species.New Phytol. 2016; 209: 798-811Crossref PubMed Scopus (53) Google Scholar, de Souza et al., 2016de Souza R.S. Okura V.K. Armanhi J.S. Jorrín B. Lozano N. da Silva M.J. González-Guerrero M. de Araújo L.M. Verza N.C. Bagheri H.C. et al.Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome.Sci. Rep. 2016; 6: 28774Crossref PubMed Scopus (23) Google Scholar, Fonseca-García et al., 2016Fonseca-García C. Coleman-Derr D. Garrido E. Visel A. Tringe S.G. Partida-Martínez L.P. The cacti microbiome: Interplay between habitat-filtering and host-specificity.Front. Microbiol. 2016; 7: 150Crossref PubMed Scopus (7) Google Scholar, Wagner et al., 2016Wagner M.R. Lundberg D.S. Del Rio T.G. Tringe S.G. Dangl J.L. Mitchell-Olds T. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant.Nat. Commun. 2016; 7: 12151Crossref PubMed Scopus (35) Google Scholar, Zarraonaindia et al., 2015Zarraonaindia I. Owens S.M. Weisenhorn P. West K. Hampton-Marcell J. Lax S. Bokulich N.A. Mills D.A. Martin G. Taghavi S. et al.The soil microbiome influences grapevine-associated microbiota.MBio. 2015; 6: e02527-14Crossref PubMed Scopus (0) Google Scholar).Fungi: ∗ gene copy numbers g−1 samples: Belowground: (Rousk et al., 2010Rousk J. Bååth E. Brookes P.C. Lauber C.L. Lozupone C. Caporaso J.G. Knight R. Fierer N. Soil bacterial and fungal communities across a pH gradient in an arable soil.ISME J. 2010; 4: 1340-1351Crossref PubMed Scopus (0) Google Scholar, Siles and Margesin, 2016Siles J.A. Margesin R. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors?.Microb. Ecol. 2016; 72: 207-220Crossref PubMed Scopus (6) Google Scholar, Trivedi et al., 2016Trivedi P. Delgado-Baquerizo M. Trivedi C. Hu H. Anderson I.C. Jeffries T.C. Zhou J. Singh B.K. Microbial regulation of the soil carbon cycle: evidence from gene-enzyme relationships.ISME J. 2016; 10: 2593-2604Crossref PubMed Scopus (6) Google Scholar); Aboveground: P.T.’s unpublished data. ‡ OTUs: Belowground: (Maestre et al., 2015Maestre F.T. Delgado-Baquerizo M. Jeffries T.C. Eldridge D.J. Ochoa V. Gozalo B. Quero J.L. García-Gómez M. Gallardo A. Ulrich W. et al.Increasing aridity reduces soil microbial diversity and abundance in global drylands.Proc. Natl. Acad. Sci. USA. 2015; 112: 15684-15689PubMed Google Scholar, Siles and Margesin, 2016Siles J.A. Margesin R. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors?.Microb. Ecol. 2016; 72: 207-220Crossref PubMed Scopus (6) Google Scholar, Trivedi et al., 2016Trivedi P. Delgado-Baquerizo M. Trivedi C. Hu H. Anderson I.C. Jeffries T.C. Zhou J. Singh B.K. Microbial regulation of the soil carbon cycle: evidence from gene-enzyme relationships.ISME J. 2016; 10: 2593-2604Crossref PubMed Scopus (6) Google Scholar); Aboveground: (Coleman-Derr et al., 2016Coleman-Derr D. Desgarennes D. Fonseca-Garcia C. Gross S. Clingenpeel S. Woyke T. North G. Visel A. Partida-Martinez L.P. Tringe S.G. Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species.New Phytol. 2016; 209: 798-811Crossref PubMed Scopus (53) Google Scholar, de Souza et al., 2016de Souza R.S. Okura V.K. Armanhi J.S. Jorrín B. Lozano N. da Silva M.J. González-Guerrero M. de Araújo L.M. Verza N.C. Bagheri H.C. et al.Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome.Sci. Rep. 2016; 6: 28774Crossref PubMed Scopus (23) Google Scholar, Fonseca-García et al., 2016Fonseca-García C. Coleman-Derr D. Garrido E. Visel A. Tringe S.G. Partida-Martínez L.P. The cacti microbiome: Interplay between habitat-filtering and host-specificity.Front. Microbiol. 2016; 7: 150Crossref PubMed Scopus (7) Google Scholar).Archaea: ∗ gene copy numbers g−1 samples: Belowground: (Siles and Margesin, 2016Siles J.A. Margesin R. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors?.Microb. Ecol. 2016; 72: 207-220Crossref PubMed Scopus (6) Google Scholar); Aboveground: (Müller et al., 2015Müller H. Berg C. Landa B.B. Auerbach A. Moissl-Eichinger C. Berg G. Plant genotype-specific archaeal and bacterial endophytes but similar Bacillus antagonists colonize Mediterranean olive trees.Front Microbiol. 2015; 6: 138Crossref PubMed Scopus (14) Google Scholar) and P.T.’s unpublished data. ‡ OTUs: Belowground: (Siles and Margesin, 2016Siles J.A. Margesin R. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors?.Microb. Ecol. 2016; 72: 207-220Crossref PubMed Scopus (6) Google Scholar); Aboveground: (Coleman-Derr et al., 2016Coleman-Derr D. Desgarennes D. Fonseca-Garcia C. Gross S. Clingenpeel S. Woyke T. North G. Visel A. Partida-Martinez L.P. Tringe S.G. Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species.New Phytol. 2016; 209: 798-811Crossref PubMed Scopus (53) Google Scholar, Fonseca-García et al., 2016Fonseca-García C. Coleman-Derr D. Garrido E. Visel A. Tringe S.G. Partida-Martínez L.P. The cacti microbiome: Interplay between habitat-filtering and host-specificity.Front. Microbiol. 2016; 7: 150Crossref PubMed Scopus (7) Google Scholar).Virus: ∗∗ Virus like particles (VLPs). Belowground: (Ashelford et al., 2003Ashelford K.E. Day M.J. Fry J.C. Elevated abundance of bacteriophage infecting bacteria in soil.Appl. Environ. Microbiol. 2003; 69: 285-289Crossref PubMed Scopus (0) Google Scholar, Williamson et al., 2005Williamson K.E. Radosevich M. Wommack K.E. Abundance and diversity of viruses in six Delaware soils.Appl. Environ. Microbiol. 2005; 71: 3119-3125Crossref PubMed Scopus (94) Google Scholar, Buée et al., 2009Buée M. De Boer W. Martin F. van Overbeek L. Jurkevitch E. The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors.Plant and Soil. 2009; 321: 189-212Crossref Scopus (0) Google Scholar) (and reference within); Aboveground: (Roossinck, 2015Roossinck M.J. A new look at plant viruses and their potential beneficial roles in crops.Mol. Plant Pathol. 2015; 16: 331-333Crossref PubMed Scopus (3) Google Scholar) (and references within). ‡‡ Belowground: Unique VLPs (Ashelford et al., 2003Ashelford K.E. Day M.J. Fry J.C. Elevated abundance of bacteriophage infecting bacteria in soil.Appl. Environ. Microbiol. 2003; 69: 285-289Crossref PubMed Scopus (0) Google Scholar, Williamson et al., 2005Williamson K.E. Radosevich M. Wommack K.E. Abundance and diversity of viruses in six Delaware soils.Appl. Environ. Microbiol. 2005; 71: 3119-3125Crossref PubMed Scopus (94) Google Scholar, Buée et al., 2009Buée M. De Boer W. Martin F. van Overbeek L. Jurkevitch E. The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors.Plant and Soil. 2009; 321: 189-212Crossref Scopus (0) Google Scholar) (and reference within); Aboveground: ‡‡‡Sequences (Roossinck, 2015Roossinck M.J. A new look at plant viruses and their potential beneficial roles in crops.Mol. Plant Pathol. 2015; 16: 331-333Crossref PubMed Scopus (3) Google Scholar) (and references within).Nematodes: ∗∗∗Number of individuals (Bardgett and van der Putten, 2014Bardgett R.D. van der Putten W.H. Belowground biodiversity and ecosystem functioning.Nature. 2014; 515: 505-511Crossref PubMed Scopus (258) Google Scholar, Mendes et al., 2013Mendes R. Garbeva P. Raaijmakers J.M. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms.FEMS Microbiol. Rev. 2013; 37: 634-663Crossref PubMed Scopus (259) Google Scholar, Kergunteuil et al., 2016Kergunteuil A. Bakhtiari M. Formenti L. Xiao Z. Defossez E. Rasmann S. Biological control beneath the Feet: A review of crop protection against insect root herbivores.Insects. 2016; 7: E70Crossref PubMed Scopus (0) Google Scholar) (and references within); ‡‡‡‡genera. (Kergunteuil et al., 2016Kergunteuil A. Bakhtiari M. Formenti L. Xiao Z. Defossez E. Rasmann S. Biological control beneath the Feet: A review of crop protection against insect root herbivores.Insects. 2016; 7: E70Crossref PubMed Scopus (0) Google Scholar) (and references within).Protists: ∗∗∗Number of individuals (Mendes et al., 2013Mendes R. Garbeva P. Raaijmakers J.M. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms.FEMS Microbiol. Rev. 2013; 37: 634-663Crossref PubMed Scopus (259) Google Scholar) (and reference within); ‡‡‡Sequences. (Bates et al., 2013Bates S.T. Clemente J.C. Flores G.E. Walters W.A. Parfrey L.W. Knight R. Fierer N. Global biogeography of highly diverse protistan communities in soil.ISME J. 2013; 7: 652-659Crossref PubMed Scopus (104) Google Scholar, Grossmann et al., 2016Grossmann L. Jensen M. Heider D. Jost S. Glücksman E. Hartikainen H. Mahamdallie S.S. Gardner M. Hoffmann D. Bass D. Boenigk J. Protistan community analysis: key findings of a large-scale molecular sampling.ISME J. 2016; 10: 2269-2279Crossref PubMed Scopus (18) Google Scholar).Arthropods: ∗∗∗Number of individuals and ‡‡‡‡‡ species (Hansen et al., 2001Hansen R.A. Williams R.S. Degenhardt D.C. Lincoln D.E. Non-litter effects of elevated CO2 on forest floor microarthropod abundances.Plant Soil. 2001; 236: 139-144Crossref Scopus (15) Google Scholar, Mendes et al., 2013Mendes R. Garbeva P. Raaijmakers J.M. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms.FEMS Microbiol. Rev. 2013; 37: 634-663Crossref PubMed Scopus (259) Google Scholar) (and references within).Earthworms: ∗∗∗number of worms and ‡‡‡‡‡ Species (Bardgett and van der Putten, 2014Bardgett R.D. van der Putten W.H. Belowground biodiversity and ecosystem functioning.Nature. 2014; 515: 505-511Crossref PubMed Scopus (258) Google Scholar, Eriksen-Hamel et al., 2009Eriksen-Hamel N.S. Speratti A.B. Whalen J.K. Legere A. Madramootoo C.A. Earthworm populations and growth rates related to long-term crop residue and tillage management.Soil Tillage Res. 2009; 104: 311-316Crossref Scopus (23) Google Scholar, Richard et al., 2012Richard B. Legras M. Margerie P. Mathieu J. Barot S. Caro G. Desjardins T. Dubs F. Dupont L. Decaëns T. Spatial organization of earthworm assemblages in pastures of northwestern France.Eur. J. Soil Biol. 2012; 53: 62-69Crossref Scopus (8) Google Scholar) (and references within).Algae: ∗∗∗ Number of cells and ‡‡‡‡‡ Species (Zancan et al., 2006Zancan S. Trevisan R. Paoletti M.G. Soil algae composition under different agro-ecosystems in North-Eastern Italy.Agr. Ecosyst. Environ. 2006; 112: 1-12Crossref Scopus (38) Google Scholar, Lin et al., 2013Lin C.S. Chou T.L. Wu J.T. Biodiversity of soil algae in the farmlands of mid-Taiwan.Bot. Stud. 2013; 54: 41-48Crossref PubMed Scopus (3) Google Scholar, Mendes et al., 2013Mendes R. Garbeva P. Raaijmakers J.M. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms.FEMS Microbiol. Rev. 2013; 37: 634-663Crossref PubMed Scopus (259) Google Scholar) (and reference within). Open table in a new tab Belowground represents soil, root, and rhizosphere regions, while aboveground represents the phyllosphere. Units can vary strongly between taxonomic groups, depending on the method of analysis, data representation, and sample collection. Numbers are indicative only, as the majority of the soil biodiversity is yet to be explored, and because most estimates are based on single ecosystems or regions. Approximate number of genes per sample−1 were calculated based on the average number of genes in the members of representative groups X average abundance. For bacteria, fungi, virus, and archaea, data on gene copies were collected from IMG-JGI. ∗ Gene copy numbers; ∗∗ virus like particles (VLPs); ∗∗∗ number of individuals ‡Operational taxonomic units (OTUs); ‡‡ Unique VLPs; ‡‡‡ Unique sequences; ‡‡‡‡ genera; ‡‡‡‡‡ species Bacteria: ∗ gene copy numbers g−1 samples: Belowground: (Rousk et al., 2010Rousk J. Bååth E. Brookes P.C. Lauber C.L. Lozupone C. Caporaso J.G. Knight R. Fierer N. Soil bacterial and fungal communities across a pH gradient in an arable soil.ISME J. 2010; 4: 1340-1351Crossref PubMed Scopus (0) Google Scholar, Siles and Margesin, 2016Siles J.A. Margesin R. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors?.Microb. Ecol. 2016; 72: 207-220Crossref PubMed Scopus (6) Google Scholar, Trivedi et al., 2016Trivedi P. Delgado-Baquerizo M. Trivedi C. Hu H. Anderson I.C. Jeffries T.C. Zhou J. Singh B.K. Microbial regulation of the soil carbon cycle: evidence from gene-enzyme relationships.ISME J. 2016; 10: 2593-2604Crossref PubMed Scopus (6) Google Scholar); Aboveground: (Williams and Marco, 2014Williams T.R. Marco M.L. Phyllosphere microbiota composition and microbial community transplantation on lettuce plants grown indoors.MBio. 2014; 5 (e01564–14)Crossref Scopus (14) Google Scholar). ‡ Operational taxonomic units (OTUs): Belowground: (Maestre et al., 2015Maestre F.T. Delgado-Baquerizo M. Jeffries T.C. Eldridge D.J. Ochoa V. Gozalo B. Quero J.L. García-Gómez M. Gallardo A. Ulrich W. et al.Increasing aridity reduces soil microbial diversity and abundance in global drylands.Proc. Natl. Acad. Sci. USA. 2015; 112: 15684-15689PubMed Google Scholar, Siles and Margesin, 2016Siles J.A. Margesin R. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors?.Microb. Ecol. 2016; 72: 207-220Crossref PubMed Scopus (6) Google Scholar, Trivedi et al., 2016Trivedi P. Delgado-Baquerizo M. Trivedi C. Hu H. Anderson I.C. Jeffries T.C. Zhou J. Singh B.K. Microbial regulation of the soil carbon cycle: evidence from gene-enzyme relationships.ISME J. 2016; 10: 2593-2604Crossref PubMed Scopus (6) Google Scholar); Aboveground: (Coleman-Derr et al., 2016Coleman-Derr D. Desgarennes D. Fonseca-Garcia C. Gross S. Clingenpeel S. Woyke T. North G. Visel A. Partida-Martinez L.P. Tringe S.G. Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species.New Phytol. 2016; 209: 798-811Crossref PubMed Scopus (53) Google Scholar, de Souza et al., 2016de Souza R.S. Okura V.K. Armanhi J.S. Jorrín B. Lozano N. da Silva M.J. González-Guerrero M. de Araújo L.M. Verza N.C. Bagheri H.C. et al.Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome.Sci. Rep. 2016; 6: 28774Crossref PubMed Scopus (23) Google Scholar, Fonseca-García et al., 2016Fonseca-García C. Coleman-Derr D. Garrido E. Visel A. Tringe S.G. Partida-Martínez L.P. The cacti microbiome: Interplay between habitat-filtering and host-specificity.Front. Microbiol. 2016; 7: 150Crossref PubMed Scopus (7) Google Scholar, Wagner et al., 2016Wagner M.R. Lundberg D.S. Del Rio T.G. Tringe S.G. Dangl J.L. Mitchell-Olds T. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant.Nat. Commun. 2016; 7: 12151Crossref PubMed Scopus (35) Google Scholar, Zarraonaindia et al., 2015Zarraonaindia I. Owens S.M. Weisenhorn P. West K. Hampton-Marcell J. Lax S. Bokulich N.A. Mills D.A. Martin G. Taghavi S. et al.The soil microbiome influences grapevine-associated microbiota.MBio. 2015; 6: e02527-14Crossref PubMed Scopus (0) Google Scholar). Fungi: ∗ gene copy numbers g−1 samples: Belowground: (Rousk et al., 2010Rousk J. Bååth E. Brookes P.C. Lauber C.L. Lozupone C. Caporaso J.G. Knight R. Fierer N. Soil bacterial and fungal communities across a pH gradient in an arable soil.ISME J. 2010; 4: 1340-1351Crossref PubMed Scopus (0) Google Scholar, Siles and Margesin, 2016Siles J.A. Margesin R. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors?.Microb. Ecol. 2016; 72: 207-220Crossref PubMed Scopus (6) Google Scholar, Trivedi et al., 2016Trivedi P. Delgado-Baquerizo M. Trivedi C. Hu H. Anderson I.C. Jeffries T.C. Zhou J. Singh B.K. Microbial regulation of the soil carbon cycle: evidence from gene-enzyme relationships.ISME J. 2016; 10: 2593-2604Crossref PubMed Scopus (6) Google Scholar); Aboveground: P.T.’s unpublished data. ‡ OTUs: Belowground: (Maestre et al., 2015Maestre F.T. Delgado-Baquerizo M. Jeffries T.C. Eldridge D.J. Ochoa V. Gozalo B. Quero J.L. García-Gómez M. Gallardo A. Ulrich W. et al.Increasing aridity reduces soil microbial diversity and abundance in global drylands.Proc. Natl. Acad. Sci. USA. 2015; 112: 15684-15689PubMed Google Scholar, Siles and Margesin, 2016Siles J.A. Margesin R. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors?.Microb. Ecol. 2016; 72: 207-220Crossref PubMed Scopus (6) Google Scholar, Trivedi et al., 2016Trivedi P. Delgado-Baquerizo M. Trivedi C. Hu H. Anderson I.C. Jeffries T.C. Zhou J. Singh B.K. Microbial regulation of the soil carbon cycle: evidence from gene-enzyme relationships.ISME J. 2016; 10: 2593-2604Crossref PubMed Scopus (6) Google Scholar); Aboveground: (Coleman-Derr et al., 2016Coleman-Derr D. Desgarennes D. Fonseca-Garcia C. Gross S. Clingenpeel S. Woyke T. North G. Visel A. Partida-Martinez L.P. Tringe S.G. Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species.New Phytol. 2016; 209: 798-811Crossref PubMed Scopus (53) Google Scholar, de Souza et al., 2016de Souza R.S. Okura V.K. Armanhi J.S. Jorrín B. Lozano N. da Silva M.J. González-Guerrero M. de Araújo L.M. Verza N.C. Bagheri H.C. et al.Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome.Sci. Rep. 2016; 6: 28774Crossref PubMed Scopus (23) Google Scholar, Fonseca-García et al., 2016Fonseca-García C. Coleman-Derr D. Garrido E. Visel A. Tringe S.G. Partida-Martínez L.P. The cacti microbiome: Interplay between habitat-filtering and host-specificity.Front. Microbiol. 2016; 7: 150Crossref PubMed Scopus (7) Google Scholar). Archaea: ∗ gene copy numbers g−1 samples: Belowground: (Siles and Margesin, 2016Siles J.A. Margesin R. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors?.Microb. Ecol. 2016; 72: 207-220Crossref PubMed Scopus (6) Google Scholar); Aboveground: (Müller et al., 2015Müller H. Berg C. Landa B.B. Auerbach A. Moissl-Eichinger C. Berg G. Plant genotype-specific archaeal and bacterial endophytes but similar Bacillus antagonists colonize Mediterranean olive trees.Front Microbiol. 2015; 6: 138Crossref PubMed Scopus (14) Google Scholar) and P.T.’s unpublished data. ‡ OTUs: Belowground: (Siles and Margesin, 2016Siles J.A. Margesin R. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors?.Microb. Ecol. 2016; 72: 207-220Crossref PubMed Scopus (6) Google Scholar); Aboveground: (Coleman-Derr et al., 2016Coleman-Derr D. Desgarennes D. Fonseca-Garcia C. Gross S. Clingenpeel S. Woyke T. North G. Visel A. Partida-Martinez L.P. Tringe S.G. Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species.New Phytol. 2016; 209: 798-811Crossref PubMed Scopus (53) Google Scholar, Fonseca-García et al., 2016Fonseca-García C. Coleman-Derr D. Garrido E. Visel A. Tringe S.G. Partida-Martínez L.P. The cacti microbiome: Interplay between habitat-filtering and host-specificity.Front. Microbiol. 2016; 7: 150Crossref PubMed Scopus (7) Google Scholar). Virus: ∗∗ Virus like particles (VLPs). Belowground: (Ashelford et al., 2003Ashelford K.E. Day M.J. Fry J.C. Elevated abundance of bacteriophage infecting bacteria in soil.Appl. Environ. Microbiol. 2003; 69: 285-289Crossref PubMed Scopus (0) Google Scholar, Williamson et al., 2005Williamson K.E. Radosevich M. Wommack K.E. Abundance and diversity of viruses in six Delaware soils.Appl. Environ. Microbiol. 2005; 71: 3119-3125Crossref PubMed Scopus (94) Google Scholar, Buée et al., 2009Buée M. De Boer W. Martin F. van Overbeek L. Jurkevitch E. The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors.Plant and Soil. 2009; 321: 189-212Crossref Scopus (0) Google Scholar) (and reference within); Aboveground: (Roossinck, 2015R
Referência(s)