Determinants of Host Species Range in Plant Viruses Benoît Moury, Frédéric Fabre, Eugénie Hébrard, Rémy Froissart

Determinants of host species range in plant viruses Benoît Moury, Frédéric Fabre, Eugénie Hébrard, Rémy Froissart

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Benoît Moury, Frédéric Fabre, Eugénie Hébrard, Rémy Froissart. Determinants of host species range in plant viruses. Journal of General Virology, Microbiology Society, 2017, 98 (4), pp.862-873. 10.1099/jgv.0.000742. hal-01522298

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Distributed under a Creative Commons Attribution - ShareAlike| 4.0 International License Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: breadth, range host relHRB:breadth. relative Non bipartite Keywords: author: Corresponding R &Ecologie, Contrôle»,Génétique, Evolution Montpellier CNRS UMR5290, (5) parasites», CampusinternationaldeBaillarguet,F INRA UMR385, (4) IRD Environnement", France Montpellier UMR186, (3) des Sciences la de Vigneet du Vin, F (2) (1) Pathologie Végétale, Moury,Fabre,(1), B. F. Hébrard, Froissart,(2), (4,5) E. R. (3), Determinants ofhost species range plantin viruses Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). unning titleunning UMR 1065 UMR - standard abbreviations:standard network

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(ii) the probabilisticdegree model, null for where

missing the same totalnumberthe ost cases inthesame data . Two Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: Not applicable statementEthical The interest of Conflict comments themanuscript. on KarineBerthier, FargetteLecoq and for Hervé thisstudy thespark of and toThierryCandress Thanks Véronique to Decognetefficientdatab forhelpinthe management of the Acknowledgments play programme of This workInfectieuses wasby supported (Maladies interdisciplinary theMIE Emergentes) Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017).

authors ofinterest. noconflict declare any role in the study orinthepreparationany articledecision role of inthe study the or topublish.

CNRS (CentreNationallaRechercheCNRS de Scientifique). Stéphane BlancStéphane

Comment citer cedocument: 10.1099/jgv.0.000742

and Julien Papaïx Papaïx and Julien

for help analyses in constructand/or

The funders funders The e, Mark Tepfer, ase

did not did not ,

to Denis to Denis ive Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: Trends Ecol Evol pathogen plants: of diseases infectious 13. pathogens 12. mastrevirusesplant hosts withtheir 11. 602. 10. evolutionary of inaplant a jump reconstruction virus host 9. of adaptability 2012 the modulate contingencies 8. range 2011 host its extend to genes nonconserved multiple acquiring 7. Microbe Interact of 6. J Gen Virol ability of 5. of plant viruses 4. 2008; 3. ecology and evolution 2. evolution ofspecies jumps 1. References Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017).

aaa igpt virus ringspot Papaya

; ; 8 108 5 : : Anderson Anderson PK MEJ Woolhouse B Wu A Gibbs N Vassilakos N Poulicard CJ Robertson S, Tatineni Chen KC N Suehiro J Dijskra Pulliam SJ Scharg DT, Haydon MEJ, Woolhouse e1002482. 80 Turnip Turnip mosaic virus : . 17366 - 91. Emerg Infect Dis Emerg Infect

2004 ,

. Melcher U Melcher . – JRC Arch Virol

, ;

. 2008 Evolution and origins of tobamoviruses of origins and Evolution 17371. 85: 2004

Chiang Chiang CH , , Importance of host ranges and other biological properties for the taxonomy the for properties biological other and ranges host of Importance

Natsuaki inr P Wiener , 2087 , . ,

Pinel . Simon V Simon ; ; framework predictive a toward Moving jumps: host Viral Cunningham AA 21 Trends Ecol Evol 19 Comment citer cedocument:

, :

: - 1046

. 535 10.1099/jgv.0.000742 2098. , Gowtage

- eemns ot pcfct fr neto o papaya of infection for specificity host determines 1992 Trends Ecol Evol az A Galzi

Guo X Guo 2005

to infect , – T .

– Raja JAJ 544. , , of roles relative the are what disease: infectious Emerging 1057. ; Tzima A Tzima Suppl5 aaae T Watanabe ; 11 . ,

- BMC Evol Biol , ane SM Garnsey : eura S Sequeria Wang X Wang 1842 Brassica Traoré O Traoré

pollution, climate change and agrotechnology drivers agrotechnology and change climate pollution, Antia :

, , 279 1995 Patel NG Liu Liu FL , - 1847. Johansen E Johansen -

2005; 289. 24 ;

10 R spp ,

Fan L L Fan

, . ie elw ote virus mottle yellow Rice kd S Okuda .

, 319 inl F Vignols

E ot ag ad mrig n reemerging and emerging and range Host

, Tai Tai CH and/or 20

merging pathogens: the epidemiology and and epidemiology the pathogens: merging , 2008 asn WO Dawson Morales Morales FJ - : 238 324. t al. et ,

; . Moury B Moury . 8 Raphanus sativus -

Phil Trans R Soc B Soc R Trans Phil .

Mol et al. 244. :

335. n motn dtriat f the of determinant important An ,

Assessment of codivergence of codivergence of Assessment Ghesquière A Ghesquière

Biol EvolBiol

13. A single amino acid of NiaPro , . Epstein Epstein PR .

. pat iu eovd by evolved virus plant A rc al cd c USA Sci Acad Natl Proc

Genetic determinism and determinism Genetic

2016

is in its P3 protein .

t al. et

; et al. 1999 LS Pathog PLOS 33 . : . 541 o Plant Mol

EcoHealth

; Emerging Historical 354 - 553. : 593

– - . .

Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: Theor Biol 27. 1987 26. viruses 25. 1990 energy activation the and constants rate of determination deamination: cytosine 24. ratesmutation across viruses 23. network: The influence asymmetric past evolutionary of history 22. Appl risk analysis: phylogenetic signal as a predictor of host range of plant pests and pathogens 21. evolve differently others? from the 20. 2012 Viruses viruses of nomenclature and 19. networks 18. and Triage SA Levin P, Kareiva In: 17. 1973 16. http://pvo.bio Database VIDE the from Lists and Descriptions Online: 15. ResVirus for prospects and conditions, world changing of effects emergence, driving factors 14. Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017).

; ; . ; 2012

25 29 54 . e S Nee A Sicard LA Frederico R Sanjuán Vacher C GS Gilbert C Desbiez King AMQ Weitz JS AG Power M Hill L Watson AJ, Gibbs MJ, Dallwitz K, Crabtree AA, Brunt RAC Jones Chao L Chao . : : : PLoS Pathog PLoS 277 2532 USA CA, Diego, San USA, MA, Waltham, UK, London, 427 .

2009 ; Trends Microbiol

5 . 1991 : Princeton, - – 869 281. - – 432. . mirror.cn/refs.htm .

2537. ;

. 141

; iest ad vnes a nfig oain n is consequences its and notation unifying a evenness: and Diversity h eouin f utcmatetl eoe i viruses in genomes multicompartmental of evolution The - Levels , , 153 , 878.

Poisot T ,

Michalakis Y Michalakis Piou D , . , , . : Moury B Moury

Flecker AS Flecker

113 Adams MJ Magarey

rm oeua gntc t pyoyais Evolutionary phylodynamics: to genetics molecular From : Plant virus emergence and evolution: origins, new encounter scenarios, encounter new origins, evolution: and emergence virus Plant 229

, 2016 USA: Princeton University Press; Kunkel TA Kunkel Comment citer cedocument: of selection, evolution of sex in RNA viruses, and the origin of life of origin the and viruses, RNA in sex of evolution selection, of –

– 130. (editors) , 246.

, 10.1099/jgv.0.000742 Desprez ; 12 Meyer JR 2013 . . ,

PLOS PathogPLOS

Ninth report of the International Committee on Taxonomy of of Taxonomy on Committee International the of report Ninth e1005819. Lecoq H Lecoq R . , ; , ,

Carstens EB ; Virus specificity in disease disease in specificity Virus now availableat: ht . 21 Gutiérrez S Gutiérrez Suiter K Suiter Inf Genet Evol The importance of species: Perspectives on Expendability on Perspectives species: of importance The , -

Loustau : Shaw BR Shaw 82 , Flores CO - . 91.

The hallmarks of "green" viruses: Do plant viruses plant Do viruses: "green" of hallmarks The ,

2012 Webb CO Webb

M 25 , , .

Lefkowitz EJ -

Blanc S Blanc A sensitive genetic assay for the detection of of detection the for assay genetic sensitive A L ;

8 2011 , . : Valverde S Architecture of an antagonistic tree/fungus e1002685. tp://sdb.im.ac.cn/vide/refs.htm; ; . 11

. 2003.

Evolutionary tools for phytosanitary for tools Evolutionary . The strange lifestyle of multipartite of lifestyle strange The : Version: 20th August 1996 August 20th Version: 812 systems: are species red species are systems: .

- Virus Virus taxonomy

pp . 824. et al. PLOS One PLOS . : 330

Elsevier Academic Press Academic Elsevier

Phage - 347. t al. et

–

2008 bacteria bacteria infection . .

. Classification ln Viruses Plant Biochemistry ; Ml Evol Mol J eeac of relevance 3 : e1740. .

1996

Ecology undant? undant? control ; . URL: URL: Evol Evol .

. J ; .

Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: Pathol host a is protein 40. 682. to resistance r hypersensitive compromise suppress differentially RCY1 thaliana Arabidopsis in 39. Chenopodium quinoa seed pea 38. different species pepper between interaction hierarchical the 37. the of tobamoviruses elicitation the for required 36. 1994 diversicaudatum Xiphinema 35. under and bothhorizontal vertical 34. virusesmultipartite 3 of plant infection thecellular virus at level. 32. progression and host 31. 1978. 30. number virus is differentiallyregulated ina multipartite 29. GenetPLOS genome segmentation can result from a trade 28. 3. Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017).

;

124 2014 Desbiez C Sekine KT K Andersen R Tomita De A laCruz CE Taylor Stewart AD J Iranzo Tromas N S Gutiérrez Maynard Smith A Sicard S Ojosnegros - : borne mosaic potyvirus modulates the ability of the virus to move systemically in in systemically move to virus the of ability the modulates potyvirus mosaic borne 469 ;

15 2011 - . 477. : Mol Plant 217 - , , specific determinant of systemic infectivity for two potyviruses two for infectivity systemic of determinant specific

, ,

, ; Yvon M Yvon , 7 Ken

Chandeysson Zwart MP , . arba SC Manrubia Ishihara Ishihara T , , - : , Proc RSoc B - 221. e1001344.

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Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: properties Table transmission vector Kind of [VEC] grouped) (arthropods Vector type Vector type transmission horizontal Abiotic [VER] transmission Vertical [SEG] segments Genome [GEN] Genome type [Variable] Virus trait Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). 1

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whitefly other fungus no vector aphid Coleoptera nematode thrips tools none graft plants contact between substrate none seed transmission >3 segments 1 segment 2 segments 3 segments dsRNA dsDNA ssDNA ssRNA Virus group non circulative transmission no vector multiplying circulative and non fungus arthropod no vector nematode

groups of of groups

Hemiptera

plant plant

- virus 22.0 ab 12. 20.2 a 10.5 b 13.5 b 15.7 b 28.3 a 3.6 b 3.9 b 12.6 a 16.7 a absHRB 14.7 a 14.7 a 16.4 a 11.3 b 14.0 b 14.4 b 33.5 a 10.9 b 11.1 b 11.3 b 14.4 b 14.8 b 15.1 ab 33.5 a 38.3 ab 10.1 ab 14.4 b 16.3 ab 16.5 a es 8

sharing genome or transmission transmission or genome sharing ‡

6 340 140 20 316 109 35 31 21 44 384 N 207 165 80 24 312 120 24 35 55 24 120 168 42 24 6 14 319 80 61

†

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(absHRB) for each virus group(absHRB) each based for virus ona

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ns , *,**,***when testsare

Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: nestedness thanthe ormodularity ‡ † Probabilistic model; PD: degree model. hypothesesthem tonull statistical simulations) assessment for (1000 * species Table

P functionsR usedtoestimate nested Modularity Nestedness Analysis Models used to fill missing data in the infectivity matrix (100 simulations)Models missing used tofill datamatrix and intheinfectivity tocompare Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). - values correspondingto the frequencymodel ofnull 2 infectivity matrix .

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Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: the average range host breadths indicated terminal node interpretedat the by top,following starting froma eachtoarrive branch each downnode, to categories: no seed, categories dsrna, dsdna variables ( properties. virus plant Fig. 1: b Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). ).

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using n: number of inthe virusspecies group.n: number r thropods weregrouped)thropods

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modelling the representingmajor biological virus set Explanatory of 293virusspecies. GEN

using a dataset of 480 virusspecies ausing datasetof ’; 4 categories: ssrna,categories: ssdna, 4 host rangehost breadth (HRB) ( variable‘VER’,

(VEC)

( variable ‘SEG’, 4 variable . T ree s

should be should

and .

of of Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI:

Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). Comment citer cedocument: 10.1099/jgv.0.000742

Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: Vitales, Pinales,Charales,Cornales, Ericales, and Geraniales Myrtales Ranunculales,Buxales, Cycadales, Proteales, Polypodiales, Dioscoreales, Saxifragales, III,II,Asparagales, Euasterids and Commelinids, Liliales, given qorder Wallis order, m of groups Fig. Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017).

host specieshost 2 :

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host s

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a species Kruskal

diversity

for afor - Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI:

Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). Comment citer cedocument: 10.1099/jgv.0.000742

Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: necrosisBYMV ( Anecrovirus), ringspot tombusvirus),PFBV ( TuMV ( potyvirus),vein mottle ( ArMV CarMV ( Chenopodium amaranticolor Spinacia oleracea Module 2contained thefollowing plantspecies: potyvirus)and ne BCTV ( ilarvirus), SLRSV ( ( species: faba Solanum tuberosum Module 1contained thefollowing plantspecies: families. identifying (delineatedgray partially three modules by lines), host of lines and (infection) correspond columns. Black to boxes andboxes hosts to white species matrix infectivity Fig. c Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). ucumbe crotic TBRV mosaic dianthovirus), ( s (noinfection). , 3 Vigna unguiculata :

Evidence of nestedness ( nestedness Evidence of b t BWYV (

urnip mosaic potyvirus), BtMVurnip mosaic potyvirus), ( c eet curly top curtovirus), PSV ( curlyeet PSV topcurtovirus), r mosaic cucumovirus), TRSV ( TRSV r mosaic cucumovirus), arnation carmovirus), mottle ( OkMV

ClYMV ( ClYMV b , eet western yellows AMVeet polerovirus), ( western Tetragonia Tetragonia s , trawberry latent sadwavirus), ringspot TRV( Gray Lactuca sativa Comment citer cedocument: , c Cucumis sativus

lover yellowlover mosaic potexvirus) boxes correspond boxes . 10.1099/jgv.0.000742 Thecorrespond two matrices thesame to dataset after permutation

and p tetragonioides a elargonium flower break flower elargonium carmovirus), TNV rabis mo rabis b a Chenopodium quinoa ean yellowean m ) and modularity) and ( ,

Brassica campestris t omato black ring nepovirus), SMV ( ringomato black SMV nepovirus), p saic nepovirus),HLV (

t b eanut cucumovirus), stunt ( RCNMV and obacco ringspot TSV ( nepovirus), eet mosaicpotyvirus),eet CymRSV ( to missinganalyses data.allowed Modularity ,

35 Phaseolus vulgaris Beta vulgaris osaic potyvirus),HVSosaic ( o

Trifolium repens Trifolium Cucurbita pepo Cucurbita kra mosaic tymovirus), CVMoV ( mosaickra tymovirus), CVMoV b ) in ) in , and thefollowingvirus species: , . Glycine max

a a ,

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obacco streak three plant ymbidium r ed clovered t obacco , c arnation arnation non , , Vicia , - Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: ( PTV ( ipomovirus),RMVmottle ( ( rustica clevelandiiNicotiana Module 3contained thefollowing plantspecies: ( ( PSbMV S), p t b obaccoCVBetch potyvirus), ( Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). hysalis mosaic tymovirus) eet necrotic yellownecrotic benyvirus) vein and p , eru potyvirus),PVMV( tomato mosaic Physalis floridana p ea seedborne mosaic potyvirus),( SqMV , Lycopersicon esculentum Comment citer cedocument:

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TEV , Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI:

Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). Comment citer cedocument: 10.1099/jgv.0.000742

Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: of15 plant speciesminimum the relHRBwas only analyzed restricted for set the ( 15 plantspecies a to goodcompromise corresponds between theprecision of HRB estimation of remaining virusspecies species (~15 which plantspecies) theincrease beyond of betweenand absHRB. relHRB for toolow aof remainingis estimationthe coefficient precise virusspecies of correlation Note species of correlation between absHRBand relHRB, precision ofestimates. HRB A coefficientbetween ofabsHRBand correlation relHRBan istherefore indicator of the HRB estimates plant species.numberspecies ofassayed Whenthe plant (relHRB)relative host range breadth To take account number into ofplant assayed thespecies total for corresponding number of tothe reported total species host isanimprecise some the hostornon InVIDE thetotalnumber the database, of range host precision of breadth (HRB)estimatesviruses number remaining and of Method S1.  Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). =0.74) ofvirus species and inthe dataset (293 remaining thenumber . Consequently, however , corresponding to a , corresponding to increases andincreases corresponds to Determination of avirus compromise of agood subset Determination with the between that when the numberthat when of - ,

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global the absolute host range host (absHRB),the absolute breadth absHRB divided by total number ofabsHRB the is observed is observed 38

plant species becomes high (>50), species the becomeshigh plant number

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plant species

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10.1099/jgv.0.000742

vi rus datasetbutmore for statistical power more 39

Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: t (PPV) istheprobability avirus classified c that inclass classif that sensitivity istheprobability thatthemodel inclass classifies c ‘ eachabsHRB the a steps were The predictive 500times. the iterated by performancesummarized modelwas of with the numbers offalse positives, negatives, true and positives true negatives the 3class dataset determined (432species) and randomlythe remaining thevirus species out10%of fittedthe (48modelto left species), predictive the performance modelwas of evaluated fitted withthefunction “clm”ofthe“ordinal” packagesoftware inthe R 3.0.2. version anywithout interaction par interaction(most VER, GEN Class_absHRB ofthe fourpropertiesfunction as mainviral a ( foundsignificant analyzed performance ofa the with logit explaining cumulative link model link species). 165 W class hosts; species), 170 2(6 to 15hosts; class 3(>15 and threeinto equilibrated of classes increasing absHRB:virusspecies), class 145 1(1to5hosts; definedWe modelsTentative thep for Method rue result positive caret Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). belongs verage sensitivity, predictive positive value specificity, andfor value negativepredictive ’ packageversion 3.0.2software, inthe R y

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Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: performance of correct bychoosinga obtained randomly). assignments class absHRB shouldbecompared Theseto ano (0.48). values the model was species),class 3( and familieshost variable Class_ 7.25 diversitygenera ofhost ord numbers oforderq=2, The rangingfrom 0.78. 0.68to (perfect discrimination). predictor.It ranges predictor thepackage using pROC. estimatedthe thearea under sensitivity compared toano used the same analysis T framework. absHRB defined variable binary a new ordinal wemodel performanceNext, testedgrouped. howthechangesand classes 3are We 2 if Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). ered variableClass_ ; 1 sameperformed analysesdiversity weregenera families the and (Hill topredict ofhost 6 0 species),class 3( and : class 1 (1 to 5 hosts; 145 virus species) 145virus class 1(1 to 5hosts; was was : class 1( are summarized inthe tables below.are summarized

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≤ Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI:

Class 3:>2.9 Class 2: Class Class1: Hill 3:> Class 2: Class Class1: Hill Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). fam gen

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Model performance index for thediversityModel families performance ofhost index Model performanc

0.56 (0.33) 0.59 (0.33) 0.45 (0.33) Sensitivity 0.46 (0.33) 0.55 (0.33) 0.36 (0.33) Sensitivity 43

e index for thediversity genera ofhost e index 0.86 (0.67) 0.54 (0.67) 0.91 (0.67) Specificity 0.82 (0.67) 0.51 (0.67) 0.86 (0.67) Specificity

0.67 (0.33) 0.38 (0.33) 0.71 (0.33) PPV 0.57 (0.33) 0.36 (0.33) 0.55 (0.33) PPV

0.79 (0.67) 0.73 (0.67) 0.77 (0.67) NPV 0.75 (0.67) 0.69 (0.67) 0.74 (0.67) NPV

Version postprint HRBreportedorderingvirus groups ofwas 1. tothat ofthe similar in terms inTable different effect (p Kruskal * relativeare HRBs on columns Methods section evennessdistribution ofthese plantgenera speciesacross families ( or wereanalyzed corresponding (columns) requirementsof numbers todifferent terms ofass in S1.Robustness between host Table ofthe links range biological breadth (HRB)estimatesproperties five species virus and of NS: nosignificant (p NS: effect N transmission vector Kind of grouped) (arthropods Vector type transmission Vertical segments Genome type Genome Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI:

- - . Wallis Wallis

value<0.05) was detectedwas value<0.05) with Kruskal Absolute and

Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017).

 n multiple multiple 293 ≥15 ). As a consequence, the resulting datasetsconsequence,). As resulting com a the /     NS

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- Wallis Wallis Hill and and Hill  gen 287 gen     n / NS . ≥15

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and 44

Hill

and and Hill fam  test; 2 gen n .     , respectively / 4 ≥15 NS ≥ 7

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Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: 293 comparisonsmultiple (p genera.generaVirus areto Kruskal lettersaccording sharing notsignificantly different † respecti * S2 Table N Mean values (absHRB) of or absolute host (relHRB) relative Begomovirus Carlavirus Comovirus Tymovirus Potyvirus Potexvirus Ilarvirus Nepovirus Virus genus Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). 293 - virus datasetconsidere were

and N vely. .

Comparison range host breadths of plant virus genera.of

480

: number of virusesgenus ofeach 12.3 b 14.1 b 16.0 ab 18.8 ab 18.8 ab 19.6 ab 28.4 ab 31.3 a (293 viruses) absHRB †

Comment citer cedocument:

value>0.05).Onlygenera containing12species virus at least inthe 10.1099/jgv.0.000742

d. 42% bc 37% c 54% abc 41% c 43% c 56% abc 71% ab 73% a (293 viruses)

relHRB

in 15 20 13 16 60 15 12 23 N

the 293 293

and 480 range breadth for different virus 9.1 b 10.8 b 15.1 ab 17.0 ab 15.5 b 14.7 ab 22.8 ab 28.7 a (480 viruses) absHRB - virus datasets,

29 31 14 18 79 23 16 26 N 480

- Wallis Wallis Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI: range breadth datasetwhich forwere (293species ≥15plantspecies assayed) with (absHRB) usingMCA dataset thewholewith a virus (480species) ofthetwo axes and MCA thepercentage variance indicated. of is by explained each axis explanatory for variables virus traits (MCA) as Fig. used Analysis sixplant MultipleCorrespondence of S1: Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). variable (relHRB) variables (relHRB)

included as illustrativevariable.included Comment citer cedocument: 10.1099/jgv.0.000742 virus host range host virus breadth.

included as illustrativevariableincluded

(b). usingtherestricted virus MCA

Variables were projectedonthe first bsolute hostrangebsolute breadth s.

absHRB and relative (a).

host host Version postprint Determinants ofhostspecies rangein plantviruses. JournalofGeneral Virology, 98(4),862-873. ,DOI:

Moury, B. (Auteurdecorrespondance), Fabre,F.,Hébrard, E.,Froissart, R.(2017). Comment citer cedocument: 10.1099/jgv.0.000742