Domestication-driven metaorganism evolution of wheat

Plants are colonized by a wide diversity of microbes including both eukaryotic and prokaryotic species. Only recently, metagenomic approaches have allowed exhaustive studies of the microbiota colonizing plant roots and above ground phyllosphere. Current research suggests that host genetics as well as a number of environmental factors are strong drivers of the phyllosphere and rhizosphere microbiota composition. So far, detailed studies have focused on the model plant species Arabidopsis thaliana. Only a few studies include experimental data of phyllosphere microbes, but these have presented evidence that the plant-associated microbiota may play a role in plant temperature and disease resistance.

Here we propose to investigate the phyllosphere microbiota of wild and domesticated wheat. A central question in our proposal is how plant domestication and cultivation has shaped the composition and genetic diversity of prokaryote and eukaryote microbes that are associated with the wheat phyllosphere. Based on studies of domesticated animals and plants, we hypothesize that domestication has decreased the diversity of microbial species and that the functional importance of phyllosphere- associated microbiota biodiversity likewise is decreased in domesticated wheat. In an evolutionary context we aim to characterize changes of the wheat microbiota over longer evolutionary times (wheat domestication and Triticum aestivum speciation, approx. 10-12,000 years ago) as well as across short evolutionary times (over 30 generations corresponding to 30 growing seasons). Our study will build upon unique collections of plant material at the center of origin of wheat, in the Near East including two wild wheat species Triticum dicoccoides and Aegilops speltoides and cultivated bread wheat Triticum aestivum. Fresh plant material will be collected not only with the purpose of extracting DNA for metagenome sequencing but also for the isolation of prokaryotic and eukaryotic symbionts (parasitic and commensals alike). Isolated and cultured organisms will be utilized for genome sequencing and functional genome analyses as well as for experimental work. In order to further investigate the stability and species specificity of microbiota associated with each wheat species we will use a synthetic phyllosphere community approach. The microbiota function will be investigated by combined inoculations of synthetic phyllosphere communities and a fungus that is pathogenic for wheat.

Our combined analysis of the prokaryotic and eukaryotic components of the wheat microbiota will serve as a first roadmap of wheat as a metaorganism, and is expected to provide novel insights into the diversity, evolution and function of the phyllosphere microbiota associated with this important crop metaorganism.


Dr. Nils Hülter

Postdoctoral Researcher, Associated Junior Researcher
Kiel University Institute for General Microbiology

Ryszard Soluch

PhD Candidate
Kiel University Institute for General Microbiology

Ezgi Özkurt

PhD Candidate
Kiel University Institute for Botany Max-Planck-Institute for Evolutionary Biology



Phylogenomic networks reveal limited phylogenetic range of lateral gene transfer by transduction.

Popa O, Landan G, Dagan T (2017); ISME J., 11(2):543-554. doi: 10.1038/ismej.2016.116

Radiofrequency catheter ablation of atrioventricular node reentrant tachycardia in children with limited fluoroscopy.

Swissa M, Birk E, Dagan T, Naimer S A, Fogelman M, Einbinder T, Bruckheimer E, Fogelman R (2017); Int J Cardiol., pii:S0167-5273(16)34000-1. doi: 10.1016/j.ijcard.2017.01.128

Evolution of Chaperonin Gene Duplication in Stigonematalean Cyanobacteria (Subsection V).

Weissenbach J, Ilhan J, Bogumil D, Hülter N, Stucken K, Dagan T (2017); Genome Biol Evol., pii:evw287. doi: 10.1093/gbe/evw287


Low biological cost of carbapenemase-encoding plasmids following transfer from Klebsiella pneumoniae to Escherichia coli.

Di Luca M C, Sørum V, Starikova I, Kloos J, Hülter N, Naseer U, Johnsen P J, Samuelsen Ø (2016); J Antimicrob Chemother, dkw350. doi: 10.1093/jac/dkw350

T4 Phage Tail Adhesin Gp12 Counteracts LPS-Induced Inflammation In Vivo.

Miernikiewicz P, Kłopot A, Soluch R, Szkuta P, Kęska W, Hodyra-Stefaniak K, Konopka A, Nowak M, Lecion D, Kaźmierczak Z, Majewska J, Harhala M, Górski A, Dąbrowska K (2016); Front Microbiol., 7:1112. doi: 10.3389/fmicb.2016.01112

Life cycle specialization of filamentous pathogens—colonization and reproduction in plant tissues.

Haueisen J, Stukenbrock E H (2016); Current Opinion in Microbiology, 32:31-37.  doi: 10.1016/j.mib.2016.04.015

DnaK-dependent accelerated evolutionary rate in prokaryotes.

Kadibelban A S, Bogumil D, Landan G, Dagan T (2016); Genome Biol Evol, 8(5):1590-9. doi: 10.1093/gbe/evw102.

The role of hybridization in the evolution and emergence of new fungal plant pathogens.

Stukenbrock E H (2016); Phytopathology, 106(2):104-112. doi: 10.1094/PHYTO-08-15-0184-RVW

Hybridization speeds up the emergence and evolution of a new pathogen species.

Stukenbrock E H (2016); Nature genetics, 48:113-115. doi: 10.1038/ng.3494


First Report of Colletotrichum fructicola as the causal agent of Anthracnose on Common Bean and Cowpea.

Atghia O, Alizadeh A, Fotouhifar K B, Damm U, Stukenbrock E H, Javan-Nikkhah M (2015); Mycol Iran., 135–136. doi: 10.22043/mi.2015.19966

New records of Colletotrichum species for the mycobiota of Iran.

Alizadeh A, Javan-Nikkhah M, Zare R, Fotouhifar K B, Damm U, Stukenbrock E H (2015); Mycol Iran., 94–108. doi: 10.22043/mi.2015.19967

Determining the origin of synchronous multifocal bladder cancer by exome sequencing.

Acar Ö, Özkurt E, Demir G, Saraç H, Alkan C, Esen T, Somel M, Lack N A (2015); BMC Cancer, 15:871. doi: 10.1186/s12885-015-1859-8

Histone modifications rather than the novel regional centromeres of Zymoseptoria tritici distinguish core and accessory chromosomes.

Schotanus K, Soyer J, Connolly L, Grandabuert J, Happel P, Smith K, Freitag M, Stukenbrock E H
(2015); Epigenetics and Chromatin, 8:41. doi: 10.1186/s13072-015-0033-5

Rapidly Evolving Genes Are Key Players in Host Specialization and Virulence of the Fungal Wheat Pathogen Zymoseptoria tritici (Mycosphaerella graminicola).

Poppe S, Dorsheimer L, Happel P, Stukenbrock E H (2015); PLoS Pathogens, 11(7). doi: 10.1371/journal.ppat.1005055

RNA-seq based gene annotation and comparative genomics of four fungal grass pathogens in the genus Zymoseptoria identify novel orphan genes and species-specific invasions of transposable elements.

Grandaubert J, Bhattacharyya A, Stukenbrock E H (2015); G3, 5:1323-1333. doi: 10.1534/g3.115.017731

The Contribution of Genetic Recombination to CRISPR Array Evolution.

Kupczok A, Landan G, Dagan T (2015); Genome Biol Evol, 7(7):1925-39. doi: 10.1093/gbe/evv113

Chromatin analyses of Zymoseptoria tritici: methods for chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-seq).

Soyer J, Möller M, Schotanus K, Connolly L R, Galazka J M, Freitag M, Stukenbrock E H (2015); Fungal Genet Biol, 79:63-70. doi: 10.1016/j.fgb.2015.03.006

Growth-phase specific evolutionary benefits of natural transformation in Acinetobacter baylyi.

Utnes A L G, Sørum V, Hülter N, Primicerio R, Hegstad R, Kloos J, Nielsen K M, Johnsen P J (2015); ISME J, 9(10):2221-31. doi: 10.1038/ismej.2015.35

Persistence of a pKPN3-like CTX-M-15-encoding IncFIIK plasmid in a Klebsiella pneumoniae ST17 host during two years of intestnal colonizaton.

Høyland-Löhr I, Hülter N, Bernhof E, Johnsen P J, Sundsford A, Naseer U (2015); PLoS One, 10(3):e0116516. doi: 10.1371/journal.pone.0116516


Heterochrony explains convergent testis evolution in primates.

Saglican E, Özkurt E, Hu H, Erdem B, Khaitovich P, Somel M (2014); bioRxiv. doi: 10.1101/010553

SMBE Satellite meeting on reticulated microbial evolution 2014–meeting report.

Dagan T, Bapteste E, McInerney J O, Martin W F (2014); Genome Biol Evol., 6(9):2206-9. doi: 10.1093/gbe/evu173

Transcriptome sequencing 
at early stage infection of the wheat pathogen Z. tritici reveals chromosomal differences in
transcription patterns and host specific gene expression.

Kellner R, Bhattacharyya A, Poppe S, Hsu T Y, Brem R B, Stukenbrock E H (2014); Genome Biol and Evol., 6(6):1353–
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Regulation of polyp-to-jellyfish transition in Aurelia aurita.

Fuchs B, Wang W, Graspeuntner S, Li Y, Insua S, Herbst E M, Dirksen P, Bohm A M, Hemmrich G, Sommer F, Domazet-Loso T, Klostermeier U C, Anton-Erxleben F, Rosenstiel P, Bosch T C, Khalturin K (2014); Curr Biol, 24(3):263-273. doi: 10.1016/j.cub.2013.12.003

Integration of two ancestral chaperone systems into one: the evolution of eukaryotic molecular chaperones in light of eukaryogenesis.

Bogumil D, Alvarez-Ponce D, Landan G, McInerney J O, Dagan T (2014); Mol Biol Evol., 31(2):410-8. doi: 10.1093/molbev/mst212


Coevolution and life cycle
specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen.

Brunner P C, Torriani S F F, Croll D, Stukenbrock E H, McDonald B A (2013); Mol Biol Evol, 30(6):
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Selection and isolation: A genomic view of speciation in fungal
plant pathogens.

Stukenbrock E H (2013); New Phytologist, 199(4):895–907. doi: 10.1111/nph.12374

Genomes of stigonematalean cyanobacteria (Subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids.

Dagan T, Roettger M, Stucken K, Landan G, Koch R, Major P, Gould S B, Goremykin V V, Rippka R, Tandeau de Marsac N, Gugger M, Lockhart P J, Allen J F, Brune I, Maus I, Pühler A, Marti W (2013); Genome Biol Evol, 5:31-44. doi: 10.1093/gbe/evs117

Cyanobacterial defense mechanisms against foreign DNA transfer and their impact on genetic engineering.

Stucken K, Koch R, Dagan T (2013); Biol Res., 46(4):373-82. doi: 10.4067/S0716-97602013000400009


The cumulative impact of chaperone mediated folding on genome evolution.

Bogumil D, Dagan T (2012); Biochemistry, 51:9941-9953. doi: 10.1021/bi3013643

Fusion of two divergent
fungal individuals led to the recent emergence of a new widespread pathogen species.

Stukenbrock E H, Christiansen F B, Hansen T H, Dutheil J Y, Schierup M H (2012); Proc.
Natl. Acad. Sci. USA., doi: 10.1073/pnas.1201403109

A population genomics perspective on the emergence and
adaptation of new plant pathogens in agro-ecosystems.

Stukenbrock E H, Bataillon T (2012); PLoS Pathog, 8(9):e1002893. 
doi: 10.1371/journal.ppat.1002893

Chaperones divide yeast proteins into classes of evolutionary rate and expression level.

Bogumil D, Landan G, Ilhan J, Dagan T (2012); Genome Biol Evol, 4:618-625. doi: 10.1093/gbe/evs025

Acquisition of a thousand eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea.

Nelson-Sathi S, Dagan T, Landan G, Janssen A, Steel M, McInerney J, Deppenmeier U, Martin W F (2012); Proc Natl Acad Sci USA, 109:20537-20542. doi: 10.1073/pnas.1209119109

Transformation and conjugal transfer of foreign genes into the filamentous multicellular cyanobacteria (subsection V) Fischerella and Chlorogloeopsis.

Stucken K, Ilhan J, Roettger M, Dagan T, Martin W F (2012); Curr Microbiol., 65(5):552-60. doi: 10.1007/s00284-012-0193-5

An evolutionary network of genes present in the eukaryote common ancestor polls genomes on eukaryotic and mitochondrial origin.

Thiergart T, Landan G, Schenk M, Dagan T, Martin W F (2012); Genome Biol Evol., 4(4):466-85. doi: 10.1093/gbe/evs018

An exported chaperone system in P. falciparum infected erythrocytes.

Külzer S, Charnaud S, Riedel J, Mandal P, Dagan T, Crabb B S, Gilson P R, Przyborski J M (2012)

Trachipleistophora hominis prodives novel insights into reductive genome evolution in eukaryotes, in press.

Heinz E, Williams T, Nakjang S, Noël C J, Swan D C, Goldberg A V, Harris SR, Weinmaier T, Markert S, Becher D, Dagan T, Schweder T, Rattei T, Hall N, Hirt RP, Embley T M (2012)

Modern endosymbiotic theory: Getting lateral gene transfer into the equation.

Martin W F, Roettger M, Kloesges T, Thiergart T, Woehle C, Gould S, Dagan T (2012); J Endocytobiosis Cell Res, 23:1-5.

Gene transfers from organelles to the nucleus: How much, what happens, and why none in Elysia?

Martin W, Hazkani-Covo E, Shavit-Greivink L, Schmitt V, Händeler K, Gould S B, Landan G, Graur D, Dagan T (2012); Journal of Endocytobiosis and Cell Research, 23:16-20.


Pathogenicity determinants in smut fungi revealed
by genome comparison.

Schirawski J, Mannhaupt G, Karin M, Brefort T, Schipper K, Doehlemann G, Di Stasio M, Rössel N, Mendoza-Mendoza A, Pester D, Müller O, Winterberg B, Meyer E, Münsterkötter M, Wong P, Walter M,
 Stukenbrock E H, Güldener U, Kahmann R (2011); Science, 330(6010):1546-1548. doi: 10.1126/science.1195330

A machine learning approach to identify hydrogenosomal proteins in Trichomonas vaginalis.

Burstein D, Gould S B, Zimorski V, Kloesges T, Kiosse F, Major P, Martin W F, Pupko T, Dagan T (2011)Eukaryot Cell., 11(2):217-28. doi: 10.1128/EC.05225-11

Trend and barriers to lateral gene transfer in prokaryotes.

Popa O, Dagan T (2011); Curr Opin Microbiol, 14(5):615-623. doi: 10.1016/j.mib.2011.07.027

The making of a new pathogen: Insights from comparative population genomics of the
domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species.

Stukenbrock E H, Bataillon T, Duthei J Y, Hansen T T, Li R, Zala M, McDonald B A, Wang J, Schierup
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, 21:2157-2166. doi: 10.1101/gr.118851.110

Red and problematic green phylogenetic signals among thousands of nuclear genes from the photosynthetic and apicomplexa-related Chromera velia.

Woehle C, Dagan T, Martin W F, Gould S B (2011); Genome Biol Evol., 3:1220-30. doi: 10.1093/gbe/evr100

Networks uncover hidden lexical borrowing in Indo-European language evolution.

Shijulal N S, List J M, Geisler H, Fangerau H, Gray R D, Martin W, Dagan T (2011); Proc Biol Sci, 278:1794-803. doi: 10.1098/rspb.2010.1917

Directed networks reveal barriers and bypasses to lateral gene transfer in prokaryotes.

Popa O, Hazkani-Covo E, Landan G, Martin W, Dagan T (2011); Genome Res, 21(4):599-609. doi: 10.1101/gr.115592.110

Networks of gene sharing among 329 proteobacterial genomes reveal differences in lateral gene transfer frequency at different phylogenetic depths.

Kloesges T, Popa O, Martin W, Dagan T (2011); Mol Biol Evol., 28(2):1057-74. doi: 10.1093/molbev/msq297

Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plackobranchus ocellatus does not entail lateral transfer of algal nuclear genes.

Wagele H, Deusch O, Handeler K, Martin R, Schmitt V, Christa G, Pinzger B, Gould S B, Dagan T, Klussmann-Kolb A, Martin W (2011); Mol Biol Evol, 28(1):699-706. doi: 10.1093/molbev/msq239


genome and chromosome evolution associated with host adaptation and speciation of the wheat
pathogen Mycosphaerella graminicola.

Stukenbrock E H, Jørgensen F G, Zala M, Hansen T T, McDonald B A, Schierup M H (2010); PLoS Genet., 6(12):e1001189. doi: 10.1371/journal.pgen.1001189

Chaperonin-dependent accelerated substitution rates in prokaryotes.

Bogumil D, Dagan T (2010); Genome Biol Evol., 2010;2:602-8. doi: 10.1093/gbe/evq044

Evolution of spliceosomal introns following endosymbiotic gene transfer.

Ahmadinejad N, Dagan T, Gruenheit N, Martin W, Gabaldón T (2010); BMC Evol Biol., 10:57. doi: 10.1186/1471-2148-10-57


Prokaryotic evolution and the tree of life are two different things.

Bapteste E, O’Malley M A, Beiko R G, Ereshefsky M, Gogarten J P, Franklin-Hall L, Lapointe F J, Dupré J, Dagan T, Boucher Y, Martin W (2009); Biol Direct, 4:34. doi: 10.1186/1745-6150-4-34

A machine-learning approach reveals that alignment properties alone can accurately predict inference of lateral gene transfer from discordant phylogenies.

Roettger M, Martin W, Dagan T (2009); Mol Biol Evol., 26(9):1931-9. doi: 10.1093/molbev/msp105

Getting a better picture of microbial evolution en route to a network of genomes.

Dagan T, Martin W (2009); Philos Trans R Soc Lond B Biol Sci., 364(1527):2187-96. doi: 10.1098/rstb.2009.0040

A proteomic survey of Chlamydomonas reinhardtii mitochondria sheds new light on the metabolic plasticity of the organelle and on the nature of the alpha-proteobacterial mitochondrial ancestor.

Atteia A, Adrait A, Brugière S, Tardif M, van Lis R, Deusch O, Dagan T, Kuhn L, Gontero B, Martin W, Garin J, Joyard J, Rolland N (2009); Mol Biol Evol., 26(7):1533-48. doi: 10.1093/molbev/msp068

Microbiology. Seeing green and red in diatom genomes.

Dagan T, Martin W (2009); Science., 324(5935):1651-2. doi: 10.1126/science.1175765


Frequent integraton of short homologous DNA tracks during Acinetobacter baylyi transformaton and infuence of transcripton and RecJ and SbcCD DNases.

Hülter N, Wackernagel W (2008); Microbiology, 154:3676-3685. doi: 10.1099/mic.0.2008/021378-0

Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution.

Dagan T, Artzy-Randrup Y, Martin W (2008); Proc Natl Acad Sci USA, 105(29):10039–10044. doi: 10.1073/pnas.0800679105

Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor.

Deusch O, Landan G, Roettger M, Gruenheit N, Kowallik K V, Allen J F, Martin W, Dagan T (2008); Mol Biol Evol., 25(4):748-61. doi: 10.1093/molbev/msn022

Double illegitmate recombinaton events integrate DNA segments through two diferent mechanisms during natural transformaton of Acinetobacter baylyi.

Hülter N, Wackernagel W (2008); Mol Microbiol., 67(5):984-995. doi: 10.1111/j.1365-2958.2007.06096.x

Evolutionary dynamics of introns in plastid-derived genes in plants: saturation nearly reached but slow intron gain continues.

Basu M K, Rogozin I B, Deusch O, Dagan T, Martin W, Koonin E V (2008); Mol Biol Evol., 25(1):111-9. doi: 10.1093/molbev/msm234


Genome history in the symbiotic hybrid Euglena gracilis.

Ahmadinejad N, Dagan T, Martin W (2007); Gene., 402(1-2):35-9. doi: 10.1016/j.gene.2007.07.023

Molecular diversity at 18 loci in 321 wild and 92 domesticate lines reveal no reduction of nucleotide diversity during Triticum monococcum (Einkorn) domestication: implications for the origin of agriculture.

Kilian B, Ozkan H, Walther A, Kohl J, Dagan T, Salamini F, Martin W (2007); Mol Biol Evol., 24(12):2657-68. doi: 10.1093/molbev/msm192

Testing hypotheses without considering predictions.

Dagan T, Martin W (2007); Bioessays., 29(5):500-3. doi: 10.1002/bies.20566

The evolution of eukaryotes.

Martin W, Dagan T, Koonin E V, Dipippo J L, Gogarten J P, Lake J A (2007); Science., 316(5824):542-3. doi: 10.1126/science.316.5824.542c

The origin of mitochondria in light of a fluid prokaryotic chromosome model.

Esser C, Martin W, Dagan T (2007); Biol Lett., 3(2):180-4. doi: 10.1098/rsbl.2006.0582

Origin and domestication of the 
fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation.

Stukenbrock E H, Banke S, Javan-Nikkhah M, McDonald B A (2007); Molecular Biology and
 Evolution, 24(2):398-411. doi: 10.1093/molbev/msl169

Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution.

Dagan T, Martin W (2007); Proc Natl Acad Sci USA, 104(3):870–875. doi: 10.1073/pnas.0606318104


Emergence of a new disease as a result of interspecific virulence
gene transfer.

Friesen T L, Stukenbrock E H, Liu Z, Meinhardt S, Ling H, Faris J F, Rasmussen J B, Solomon P S, 
McDonald B A, Oliver R P (2006); Nature Genetics, 38:953-956. doi: 10.1038/ng1839

The “domino theory” of gene death: gradual and mass gene extinction events in three lineages of obligate symbiotic bacterial pathogens.

Dagan T, Blekhman R, Graur D (2006); Mol Biol Evol., 23(2):310-6. doi: 10.1093/molbev/msj036


The comparative method rules! Codon volatility cannot detect positive Darwinian selection using a single genome sequence.

Dagan T, Graur D (2005); Mol Biol Evol., 22(3):496-500. doi: 10.1093/molbev/msi033

GC composition of the human genome: in search of isochores.

Cohen N, Dagan T, Stone L, Graur D (2005); Mol Biol Evol., 22(5):1260-72. doi: 10.1093/molbev/msi115


Minimal conditions for exonization of intronic sequences: 5′ splice site formation in alu exons.

Sorek R, Lev-Maor G, Reznik M, Dagan T, Belinky F, Graur D, Ast G (2004);
Mol Cell., 14(2):221-31. doi: 10.1016/S1097-2765(04)00181-9

AluGene: a database of Alu elements incorporated within protein-coding genes.

Dagan T, Sorek R, Sharon E, Ast G, Graur D (2004); Nucleic Acids Res., 32:D489-92. doi: 10.1093/nar/gkh132


pANT: a method for the pairwise assessment of nonfunctionalization times of processed pseudogenes.

Fleishman S J, Dagan T, Graur D (2003); Mol Biol Evol., 20(11):1876-80. doi: 10.1093/molbev/msg202


Ratios of radical to conservative amino acid replacement are affected by mutational and compositional factors and may not be indicative of positive Darwinian selection.

Dagan T, Talmor Y, Graur D (2002); Mol Biol Evol., 19(7):1022-5. doi: 10.1093/oxfordjournals.molbev.a004161