Fusarium

Fusarium Link, Mag. Gesell. naturf. Freunde, Berlin 3(1-2): 10 (1809)

Fusarium is a genus with 20 monophyletic species complexes (Rana et al. 2017). Species formerly belonged to F. solani species complex were transferred to genus Neocosmospora based on sexual morph characters and molecular phylogeny (Lombard et al. 2015; Sandoval-Denis & Crous (2018). Fusarium species are saprobes, parasites, endophytes, soil-borne or isolated from water (Rana et al. 2017). Species of Fusarium are economically important fungi as they are responsible for blights, cankers, rots, and wilts of horticultural, ornamental and forest crops in both agricultural and natural ecosystems, worldwide, and also human infections (Rana et al. 2017; Varela et al. 2013; Peraldi et al. 2013; Al-Hatmi et al. 2019; Maryani et al. 2019a, b). In nature, sexual morphs of Fusarium occur less commonly than the asexual morphs (Gräfenhan et al. 2011; Rossman et al. 1999).

 Classification Sordariomycetes, Hypocreomycetidae, Hypocreales, Nectriaceae

Type speciesFusarium sambucinum Fuckel, Hedwigia 2: 135.1863.

Distribution – Worldwide

Disease symptoms – blights, cankers, rots, and wilts

Plant pathogenic species of this genus have the capability to change their lifestyle to saprotrophic and can survive for long periods as chlamydospores in host tissues. Fusarium species damage their hosts by systemically colonizing and occluding the host xylem (Ploetz et al. 2003).

Hosts – Known from many host plant families.

 

Morphological based identification and diversity

Fusarium was also known from the sexual morphic fungus name Gibberella, which was suppressed in favour of Fusarium by Rossman et al. (2013). Currently, 1,552 Fusarium epithets are listed in Index Fungorum (2019). Variation and mutation in culture and lack of clear morphological characters for separating species are the main problems which make the species concept of Fusarium much broader (Geiser et al. 2004). It leads to the incorrect and confusing application of species names to toxigenic and pathogenic isolates (Geiser et al. 2004). Species boundaries have been inferred using multi-gene phylogenetic methods, reflecting the species diversity more than morphological treatments (Aoki and O’Donnell 1999; Geiser et al. 2004; O’Donnell 2000; O’Donnell et al. 1998a, b; Ward et al. 2002). A combined phylogenetic analysis of LSU, ITS, RPB2 and new phylogenetic marker acl1 by Gräfenhan et al. (2011), revealed that the early concept of Fusarium is not monophyletic. Fusarium sensu Wollenweber divided into two large groups, basal ‘Fusarium-like clades’, and the other one terminal ‘Fusarium clade’ in the Nectriaceae (Gräfenhan et al. 2011).

Fig. Sexual morph of a Fusarium sp. a Herbarium material. b Ascomata on the host. c Section of ascomata. d Section of the ostiolar region. e Peridium in face view. f–h Asci (h in Melzer’s reagent). i, j Ascospores. k Germinating ascospore. l, m Colony on MEA. Scale bars: c = 100 µm, d = 50 µm, e–k = 20 µm.

 

Molecular based identification and diversity

ITS and LSU are least informative in species-level identification of Fusarium (O’Donnell et al. 2008a; Hyde et al. 2014). Moreover, non-orthologous copies of the ITS2, which can lead to wrong phylogenetic inferences, can be detected in many species of Fusarium (Geiser et al. 2004; O’Donnell et al. 1998). Generally, for the species-level identification of fungi intron-rich regions of protein-coding genes are used as the markers (Geiser et al. 2004). The translation elongation factor 1-a (tef1), which lacks non-orthologous copies of the gene, is highly informative at the species level in Fusarium (Geiser et al. 2004). RPB1 and RPB2 are also very informative gene regions for species identification of Fusarium (O’Donnell et al. 2013; Hyde et al. 2014). Lombard et al. (2018) observed that tef1 and RPB2 genes provide better resolution of the species in the F. oxysporum complex than cmdA and tub2.

Recommended genetic markers (genus level) – ATP citrate lyase (acl1), tef1 and ITS

Recommended genetic markers (species level) – calmodulin-encoding gene (cmdA), tub2, tef1, RPB1 and RPB2

Accepted number of species: There are 1552 species epithets in Index Fungorum (2019) under this genus. More than 175 species have DNA sequence data.

References: Booth 1971, Rossman et al. 1999 (morphology), Rana et al. 2017, Gräfenhan et al. 2011; Laurence et al 2014; Lombard et al. 2018, 2019; Maryani et al. 2019a, b; Wang et al. 2019; Nalim et al. 2011(morphology, phylogeny).

Table Details of the Fusarium isolates used in the phylogenetic analyses. Ex-type (ex-epitype) strains are in bold and marked with an asterisk* and voucher strains are in bold.

Species Isolate/Voucher No RPB1 RPB2 tef1
Fusarium anguioides NRRL 25385*; ATCC 66485 JX171511 JX171624 MH742689
F. acaciae-mearnsii NRRL 26755 KM361640 KM361658 AF212449
F. acuminatum NRRL 36147; CBS 109232 HM347174 GQ505484 GQ505420
F. agapanthi NRRL 54463* KU900620 KU900625 KU900630
F. albidum NRRL 22152 JX171492 JX171605
F. albosuccineum NRRL 20459 JX171471 JX171585
F. algeriense NRRL 66647*; CBS 142638; IL-79 MF120488 MF120499
F. ananatum CBS 118516* LT996188 LT996137 KU604416
F. andiyazi NRRL 31727; CBS 119857 LT996189 LT996138 KP662901
F. anthophilum NRRL 13602; CBS 737.97 LT996190 LT996139 KU711685
F. arcuatisporum CGMCC3.19493*; LC12147 MK289799 MK289739 MK289584
F. armeniacum NRRL 6227 JX171446 JX171560 HM744692
F. asiaticum NRRL 13818*; CBS 110257 JX171459 JX171573 AF212451
F. avenaceum NRRL 54939 JX171551 JX171663 MH582391
F. aywerte NRRL 25410 JX171513 JX171626 KU171717
F. babinda NRRL 25539; CBS 396.96 JX171519 JX171632 MH742712
F. begoniae CBS 403.97*; NRRL 25300 LT996191 LT996140 AF160293
F. beomiforme NRRL 25174; CBS 740.97 JX171619
F. brachygibbosum NRRL 13829 JX171460 JX171574
F. buharicum NRRL 13371; CBS 796.70 JX171449 JX171563
F. bulbicola NRRL 13618*; CBS 220.76 KF466394 KF466404 KF466415
F. burgessii CBS 125537*; RBG 5319 KJ716217 HQ646393 HQ667149
F. callistephi CBS 187.53* MH484905 MH484966
F. carminascens CBS 144738*; CPC 25800 MH484937 MH485028
F. celtidicola MFLUCC 16-0751* MH576580
F. citri CGMCC3.19467*; LC6896 MK289828 MK289771 MK289617
F. citricola CBS 142421*; CPC 27805 LT746290 LT746310 LT746197
F. coicis NRRL 66233*; RBG5368 KP083269 KP083274 KP083251
F. commune NRRL 28387 JX171638 KU171720
F. concentricum NRRL 25181*; CBS 450.97 LT996192 JF741086 AF160282
F. concolor NRRL 13459*; CBS 961.87 JX171455 JX171569 MH742681
F. contaminatum CBS 114899* MH484901 MH484992
F. continuum F201128 KM520389 KM236780 KM236720
F. convolutans CBS 144207*; CPC 33733 LT996193 LT996141 LT996094
F. cugenangense InaCCF984* LS479560 LS479308
F. culmorum NRRL 25475; CBS 417.86 JX171515 JX171628 KY873384
F. cuneirostrum NRRL 31104 EU329558 EF408413
F. curvatum CBS 238.94; NRRL 26422; PD 94/184 MH484893 MH484984
F. cyanostomum NRRL 53998 JX171546 JX171658
F. dactylidis NRRL 29298* KM361654 KM361672 DQ459748
F. denticulatum NRRL 25302; CBS 735.97 LT996195 LT996143 AF160269
F. desaboruense InaCC F950 LS479870 LS479852
F. dlaminii NRRL 13164*; CBS 119860 KU171681 KU171701 MK639039
F. duoseptatum InaCC F916* LS479495 LS479239
F. elaeidis CBS 217.49*; NRRL 36358 MH484870 MH484961
F. enterolobii CPC 27190 LT746312 LT746199
F. equiseti NRRL 13405 GQ915491 GQ915507
F. fabacearum CBS 144743*; CPC 25802 MH484939 MH485030
F. ficicrescens CBS 125178* KT154002 KP662899
F. flocciferum NRRL 25473 JX171514 JX171627
F. foetens NRRL 38302 JX171540 JX171652 GU170559
F. fracticaudum CMW 252374 LT996196 LT996144 KJ541059
F. fractiflexum NRRL 28852* LT575064 AF160288
F. fredkrugeri CBS 144209*; CPC 33747 LT996199 LT996147 LT996097
F. fujikuroi NRRL 13566 JX171456 JX171570
F. gaditjirrii NRRL 45417 JX171654 KU171724
F. gamsi CBS 143610*; CPC 30862; OrSaAg4 LT970760 LT970788
F. globosum NRRL 26131*; CBS 428.97 KF466396 KF466406 KF466417
F. glycines CBS 144746*; CPC 25808 MH484942 MH485033
F. gossypinum CBS 116613* MH484909 MH485000
F. graminearum NRRL 31084; CBS 123657 JX171531 JX171644 HM744693
F. grosmichelii InaCC F833* LS479548 LS479295 LS479744
F. guilinense CGMCC3.19495*; LC12160 MK289831 MK289747 MK289594
F. guttiforme NRRL 22945 JX171505 JX171618
F. hainanense  CGMCC3.19478*; LC11638 MK289833 MK289735 MK289581
F. heterosporum NRRL 20693; CBS 720.79 JX171480 JX171594
F. hexaseptatum InaCC F866* LS479359 LS479805
F. hoodiae CBS 132474* MH484929 MH485020
F. hostae NRRL 29889 JX171527 JX171640 AY329034
F. inflexum NRRL 20433 JX171583 AF008479
F. ipomoeae CGMCC3.19496*; LC12165 MK289859 MK289752 MK289599
F. iranicum CBS 143608*; CPC 30860; OrSaAg2 LT970757 LT970785
F. irregulare CGMCC3.19489*; LC7188 MK289863 MK289783 MK289629
F. kalimantanense InaCC F917* LS479497 LS479241 LS479690
F. konzum CBS 119849* LT996200 LT996148 LT996098
F. kotabaruense InaCC F963* LS479875 LS479859 LS479445
F. kuroshium CBS 142642*; UCR3641 KX262236 KX262256 KX262216
F. kyushuense NRRL 25349 GQ915492 GQ915508
F. lacertarum NRRL 20423; CBS 130185 HM347137 JX171581 GQ505593
F. lactis NRRL 25200*; CBS 411.97 LT996201 LT996149 AF160272
F. langsethiae NRRL 54940 JX171550 JX171662
F. languescens CBS 645.78*; NRRL 36531 MH484880 MH484971
F. lateritium NRRL 13622 JX171457 JX171571 AY707173
F. libertatis CBS 144749*; CPC 28465 MH484944 MH485035
F. longipes NRRL 13368 JX171448 JX171562
F. luffae CGMCC3.19497*; LC12167 MK289869 MK289754 MK289601
F. lumajangense InaCC F872* LS479850 LS479441
F. lyarnte NRRL 54252; CBS 125536 JX171549 JX171661
F. mangiferae NRRL 25226*; BBA 69662 JX171509 JX171622
F. miscanthi NRRL 26231 JX171634 KU171725
F. mundagurra NRR L66235*; RBG5717 KP083272 KP083276 MK639058
F. nanum CGMCC3.19498*; LC12168 MK289871 MK289755 MK289602
F. napiforme CBS 748.97*; NRRL 13604 HM347136 EF470117 KU604409
F. nelsonii NRRL 13338 JX171447 JX171561 GQ505402
F. newnesense NRRL 66237; RBG5443 KP083271 KP083277 KJ397074
F. nirenbergiae CBS 840.88* MH484887 MH484978
F. nisikadoi NRRL 25179; CBS 742.97 JX171507 JX171620
F. nurragi NRRL 36452; CBS 392.96 JX171538 JX171650
F. nygamai NRRL 13448*; CBS 749.97 LT996202 EF470114 AF160273
F. odoratissimum InaCC F822* LS479618 LS479386
F. oligoseptatum NRRL 62579*; FRC S-2581; MAFF 246283; CBS 143241 KC691596 KC691656 KC691538
F. oxysporum CBS 144134* MH484953 MH485044
F. palustre NRRL 54056* KT597718 KT597731
F. paranaense CML1830* KF680011 KF597797
F. parvisorum CBS 137236*; FCC 5407; CMW 25267 LT996150 KJ541060
F. pernambucanum MUM 1862*; URM 7559 MH668869
F. petersiae CBS 143231* MG386139 MG386150 MG386159
F. pharetrum CBS 144751*; CPC 30824 MH484952 MH485042
F. phialophorum  InaCC F971* LS479545 LS479292 LS479741
F. phyllophilum NRRL 13617*; CBS 216.76 KF466399 KF466410 KF466421
F. pisi NRRL 22278 EU329501 AF178337
F. poae NRRL 13714 JX171458 JX171572
F. praegraminearum NRRL 39664* KX260125 KX260126 KX260120
F. proliferatum NRRL 22944; CBS 217.76 JX171504 JX171617
F. pseudensiforme NRRL 46517 KC691615 KC691645 KC691555
F. pseudocircinatum NRRL 22946*; CBS 449.97 LT996204 LT996151 AF160271
F. pseudograminearum NRRL 28062*; CBS 109956 JX171524 JX171637 AF212468
F. pseudonygamai NRRL 13592*; CBS 417.97 LT996205 LT996152 AF160263
F. purpurascens InaCC F886* LS479385 LS479827
F. ramigenum NRRL 25208*; CBS 418.98 KF466401 KF466412 KF466423
F. redolens NRRL 22901; CBS 743.97 KU171708 KU171728
F. riograndense HCF3* KX534003 KX534002
F. roseum NRRL 22187 JX171493 JX171606
F. sacchari NRRL 13999; CBS 223.76 JX171466 JX171580 KU711669
F. salinense CBS 142420*; CPC 26973 LT746286 LT746306 LT746193
F. sangayamense InaCC F960* LS479537 LS479283
F. sarcochroum NRRL 20472; CBS 745.79 JX171472 JX171586
F. scirpi NRRL 13402 JX171452 JX171566 GQ505592
F. sibiricum NRRL 53430* HQ154472 HM744684
F. siculi CBS 142422*; CPC 27188 LT746299 LT746327 LT746214
F. sororula CBS 137242* LT996206 LT996153
F. sporotrichioides NRRL 3299 JX171444 JX171558 HM744665
F. staphyleae NRRL 22316 JX171496 JX171609 MH582426
F. stercicola CBS 142481*; DSM 106211 KY556552 KY556524
F. stilboides NRRL 20429; ATCC 15662 JX171468 JX171582
F. subglutinans NRRL 22016*; CBS 747.97 JX171486 JX171599 HM057336
F. sublunatum NRRL 13384*; CBS 189.34 JX171451 JX171565
F. subtropicale NRRL 66764*; CBS 144706 MH706972 MH706973 MH706974
F. succisae NRRL 13613; CBS 219.76 LT996207 LT996154 AF160289
F. sudanense CBS 454.97*; NRRL 25451 LT996208 LT996155 KU711697
F. sulawesiense InaCC F940* LS479855 LS479443
F. tanahbumbuense InaCC F965* LS479877 LS479863 LS479448
F. tardichlamydosporum InaCC F958* LS479280 LS479729
F. tardicrescens NRRL 36113* LS479474 LS479217 LS479665
F. terricola CBS 483.94* LT996209 LT996156 KU711698
F. thapsinum NRRL 22045; CBS 733.97 JX171487 JX171600 AF160270
F. tjaetaba NRRL66243*; RBG5361 KP083267 KP083275 KP083263
F. tjaynera NRRL66246*; RBG5367 KP083268 KP083279
F. torreyae NRRL 54149 JX171548 HM068359 HM068337
F. torulosum NRRL 22748; NRRL 13919 JX171502 JX171615
F. transvaalense CBS 144211*; CPC 30923 LT996210 LT996157 LT996099
F. tricinctum NRRL 25481*; CBS 393.93 JX171516 HM068327 MH582379
F. triseptatum CBS 258.50*; NRRL 36389 MH484873 MH484964
F. udum NRRL 22949; CBS 178.32 LT996220 LT996172 AF160275
F. venenatum CBS 458.93* KM232382 KM231942
F. verrucosum NRRL 22566, BBA 64786 JX171613
F. verticillioides NRRL 20956 JX171485 JX171598
F. veterinarium CBS 109898*; NRRL 36153 MH484899 MH484990
F. volatile CBS 143874* LR596006 LR596007
F. witzenhausenense CBS 142480* KY556553 KY556525
F. xylarioides NRRL 25486; CBS 258.52 JX171517 JX171630 AY707136
F. caatingaense MUM 1859*; URM 6779 MH668845 LS398495 LS398466
F. goolgardi NRRL 66250*; RBG5411 KP083270 KP083280 KP101123
F. humuli CGMCC3.19374*; CQ1039 MK289840 MK289724 MK289570
Fusicolla aquaeductuum NRRL 20686* JX171476 JX171590

Fig. Phylogram generated from RAxML analysis based on combined RPB1, RPB2 and tef1 sequences of accepted species of Fusarium. Related sequences were obtained from GenBank. One hundred sixty-five taxa are included in the analyses, which comprise 3980 characters including gaps. Single gene analyses were carried out and compared with each species, to compare the topology of the tree and clade stability. The tree was rooted in Fusicolla aquaeductuum (NRRL 20696). Tree topology of the ML analysis was similar to the BYPP. The best scoring RAxML tree with a final likelihood value of -63956.723151 is presented. The matrix had 2254 distinct alignment patterns, with 25.13% of undetermined characters or gaps. Estimated base frequencies were as follows; A = 0.257298, C = 0.251723, G = 0.248896, T = 0.242083; substitution rates AC = 1.366599, AG = 4.760724, AT = 1.266971, CG = 0.903914, CT = 9.564945, GT = 1.000000; gamma distribution shape parameter α = 1.089091. RAxML and maximum parsimony bootstrap support value ≥70% are shown near the nodes. The scale bar indicates 0.07 changes. The ex-type strains are in bold.

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