Alternaria Nees, Syst. Pilze (Würzburg): 72 (1816) [1816–17]

For synonyms see Index Fungorum (2018)


Alternaria was established by Nees von Esenbeck (1816) and species of Alternaria are known as serious plant pathogens (Nishimura et al. 1978; Peever et al. 2002; Thomma 2003; Lawrence et al. 2013; Woudenberg et al. 2013, 2015) and saprobes (Wanasinghe et al. 2018). Alternaria species have been also recorded as endophytes in grasses, angiosperms, rice and other herbaceous plants and shrubs (Fisher and Petrini 1992; Schulz et al. 1993; Rosa et al. 2009; Polizzotto et al. 2012) and they have been also isolated from soil (Hong and Pryor 2004). Many Alternaria species are saprobic on a variety of plant tissues in different habitats (Thomma 2003; Liu et al. 2015; Wanasinghe et al. 2018). Some Alternaria species, such as A. alternata, produce host-specific toxins (Hyde et al. 2018a). Several taxa are also important postharvest pathogens, e.g. A. alternata and A. solani (El-Goorani and Sommer 1981; Reddy et al. 2000), or airborne allergens causing upper respiratory tract infections and asthma in humans (Mitakakis et al. 2001; Woudenberg et al. 2015; Hyde et al. 2018a). Mycotoxins produced by Alternaria have been found in many crops including grapevine, olive, orange and tomato (Logrieco et al. 2003). This genus has been considered as one of the most important phytopathogens, especially in temperate regions (Ariyawansa et al. 2015; Wanasinghe et al. 2018).

ClassificationDothideomycetes, Pleosporomycetidae, Pleosporales, Pleosporaceae

Type speciesAlternaria alternata (Fr.) Keissl., Beih. bot. Zbl., Abt. 2 29: 434 (1912)

Distribution – Worldwide

Disease symptoms – Leaf blotch, leaf spot, stem canker and stem end rots

Alternaria generally infects the aerial parts of its host. On leafy vegetables the infection typically starts as a small, circular, dark spot. As the disease progresses, the circular spots may enlarge and are usually gray, gray-tan or near black in colour. In some cases the spots may develop in a target pattern of concentric rings and if the host leaves are large enough unrestricted symptom development can be observed. The lesion may often be covered with a fine, black, fuzzy growth (Agrios 1997). On roots, tubers, stems and fruits dark brown to black sunken lesions with concentric rings may occur. Lesions enlarge and may girdle the stem, eventually killing the plant. Fruits that are harvested from infested plants have brown or black necrotic sunken lesions (Agrios 1997; Wenneker et al. 2018). The above symptoms can be observed when the infection is caused by A. alternata, A. arborenses, A. tenuissima (Diskin et al. 2017). Alternaria brassicola produces black sooty coloured spores within the leaf spot (Kreis et al. 2016). Purple blotch disease of Allium sp. is caused by A. porri, which initially appears as small whitish necrotic lesions on leaves, becoming large, sunken and subsequently turning brown and dark (Hahuly et al. 2018).

Hosts – Has a wide range of hosts including the families Amarylidaceae, Apiaceae, Brassicaceae, Fabaceae, Lamiaceae, Rosaceae, Rutaceae, Solanaceae, Vitaceae plus many ornamental plants and a number of weeds (Farr and Rosmann 2018).

Morphological based identification and diversity

The asexual morphs of Alternaria are ubiquitous in different environments and characterized by distinct, single, simple or irregular, loosely branched, solitary conidiophores, which may be in fascicles, and by the production of dark coloured phaeodictyospores in chains, the conidia often having a beak of tapering apical cells (Woudenberg et al. 2013). Sexual morphs have small, globose to ovoid, dark brown, papillate ostiolate ascomata, mostly 8-spored, bitunicate asci with a pedicel and ocular chamber, and muriform ascospores (e.g. section Crivellia, Eureka, Infectoria; Woudenberg et al. 2013; Ariyawansa et al. 2015a; Wanasinghe et al. 2018). Neergaard (1945) divided Alternaria into three major sections, Brevicatenatae, Longicatenatae and Noncatenatae, based on conidial catenation. However, this division is unreliable as catenation is affected by growth conditions. Simmons (1992, 1995) arranged several species groups within Alternaria based on the morphological similarity among species,. Some other genera, such as Stemphylium (Wallroth 1833) and Ulocladium (Preuss 1851) also produce phaeodictyosporic conidia and are morphologically similar to Alternaria, and this has further led to taxonomic complications. Simmons (2007) revised Alternaria taxonomy based on morphology and 275 species were recognized. At the same time, Simmons (2007) proposed three new genera Alternariaster, Chalastospora and Teretispora, for some species that were previously described in Alternaria. The Alternaria complex currently comprises 24 sections and six monophyletic lineages (Woudenberg et al. 2013).

            Colony and conidial morphology are the primary characters to identify species within this genus (Ellis 1971, 1976; Simmons 1992). Conidia in some sections are mostly dictyosporous, e.g. Alternata and Japonicae, while some are mostly phragmosporous, e.g. Alternantherae and Nimbya. Species in some sections have long apical narrow beaks or secondary conidiophores, e.g. Alternantherae, Dianthicola and Porri, while such characters are absent in other sections, e.g. Chalastospora, Gypsophilae and Ulocladium. However, in some sections overlapping conidial morphology is observed, which makes identification of Alternaria based on morphology challenging. For example, dictyospores and phragmospores can be found in the same section, such as Infectoriae and Phragmosporae. Therefore, the use of DNA sequence data is very important in resolving Alternaria taxonomy.


Molecular based identification and diversity

Molecular phylogeny has revealed multiple polyphyletic taxa within Alternaria and Alternaria species clades, which do not always correlate to morphological species-groups (Inderbitzin et al. 2006; Runa et al. 2009; Lawrence et al. 2012). Pryor and Gilbertson (2000) elucidated relationships among Alternaria, Stemphylium and Ulocladium based on ITS and SSU sequence data and revealed that Stemphylium species were phylogenetically distinct from Alternaria and Ulocladium species. Most Alternaria and Ulocladium clustered together in a large Alternaria/Ulocladium clade (Pryor and Gilbertson 2000). Chou and Wu (2002) confirmed that filament-beaked Alternaria species constitute a monophyletic group distinct from the other members in this genus and hypothesized that this group is evolutionary distinct based on ITS sequence based phylogenies. Two new species groups, A. panax and A. gypsophilae were introduced by Lawrence et al. (2013) with phylogenetic evidence, and they accepted eight well supported asexual species-sections within Alternaria, while the taxa with known sexual morphs, the A. infectoria species-groups, were not given similar rank. Woudenberg et al. (2013) delineated taxa within Alternaria and allied genera based on SSU, LSU, ITS, GAPDH, RPB2 and TEF1- α sequence data. The generic circumscription of Alternaria was emended and 24 internal clades in the Alternaria complex were treated as sections, together with six monotypic lineages. Ariyawansa et al. (2015a) revised the classification of Pleosporaceae with a major focus on Alternaria and allied genera. Agreeing with Woudenberg et al. (2013), six monotypic lineages and 24 internal clades were recognized, with Xenobotryosphaeria clustering within A. infectoria. The present study reconstructs the phylogeny of Alternaria based on analyses of a combined SSU, LSU, RPB2, ITS, GAPDH and TEF1-α sequence data. The phylogenetic tree is updated with recently introduced Alternaria species, and the resulting tree corresponds to previous studies (Woudenberg et al. 2013; Ariyawansa et al. 2015a; Thambugala et al. 2017).

Recommended genetic markers (Genus level) – LSU and SSU

Recommended genetic markers (Species level) – ITS, GAPDH, RPB2 and TEF1-α

GAPDH is the common species marker used in identification of Alternaria species. Combined GAPDH with ITS, RPB2 and TEF1- α provides satisfactory resolution for resolving species.

Accepted number of species: There are 730 species epithets in Index Fungorum (2018) under this genus. However, only 87 have DNA sequence data.

References: Simmons 2007 (morphology), Ariyawansa et al. 2015a, Lawrence et al. 2013, Woudenberg et al. 2013, 2015 (morphology, phylogeny).

Table  Details of the Alternaria isolates used in the phylogenetic analyses.

Species name Strain number GenBank accession numbers
Alternaria abundans CBS 534.83 KC584581 KC584323 KC584448 JN383485 KC584154 KC584707
A. alternantherae CBS 124392 KC584506 KC584251 KC584374 KC584179 KC584096 KC584633
A. alternariae CBS 126989 KC584604 KC584346 KC584470 AF229485 AY278815 KC584730
A. alternate CBS 916.96 KC584507 DQ678082 KC584375 AF347031 AY278808 KC584634
A. arborescens CBS 102605 KC584509 KC584253 KC584377 AF347033 AY278810 KC584636
A. argyranthemi CBS 116530 KC584510 KC584254 KC584378 KC584181 KC584098 KC584637
A. arrhenatheri BMP 0514 JQ693680 JQ693629
A. aspera CBS 115269 KC584607 KC584349 KC584474 KC584242 KC584166 KC584734
A. atra CBS 195.67 KC584608 KC584350 KC584475 AF229486 KC584167 KC584735
A. axiaeriisporifera CBS 118715 KC584513 KC584257 KC584381 KC584184 KC584101 KC584640
A. bornmueller DAOM 231361 KC584624 KC584366 KC584491 FJ357317 FJ357305 KC584751
A. botryospora CBS 478.90 KC584594 KC584336 KC584461 AY278844 AY278831 KC584720
A.  botrytis CBS 197.67 KC584609 KC584351 KC584476 KC584243 KC584168 KC584736
A. brassicae CBS 116528 KC584514 KC584258 KC584382 KC584185 KC584102 KC584641
A. brassicae- pekinensis CBS 121493 KC584611 KC584353 KC584478 KC584244 KC584170 KC584738
A. brassicicola CBS 118699 KC584515 KC584259 KC584383 JX499031 KC584103 KC584642
A. breviramosa CBS 121331 KC584574 KC584318 KC584442 FJ839608 KC584148 KC584700
A. calycipyricola CBS 121545 KC584516 KC584260 KC584384 KC584186 KC584104 KC584643
A. capsici-annui CBS 504.74 KC584517 KC584261 KC584385 KC584187 KC584105 KC584644
A. caricis CBS 480.90 KC584600 KC584342 KC584467 AY278839 AY278826 KC584726
A. carotiincultae CBS 109381 KC584518 KC584262 KC584386 KC584188 KC584106 KC584645
A. cetera CBS 121340 KC584573 KC584317 KC584441 JN383482 AY562398 KC584699
A. chartarum CBS 200.67 KC584614 KC584356 KC584481 AF229488 KC584172 KC584741
A. cheiranthi CBS 109384 KC584519 KC584263 KC584387 AF229457 KC584107 KC584646
A. chlamydospora CBS 491.72 KC584520 KC584264 KC584388 KC584189 KC584108 KC584647
A. chlamydosporigena CBS 341.71 KC584584 KC584326 KC584451 KC584231 KC584156 KC584710
A. cinerariae CBS 116495 KC584521 KC584265 KC584389 KC584190 KC584109 KC584648
A. concatenate CBS 120006 KC584613 KC584355 KC584480 KC584246 AY762950 KC584740
A. conjuncta CBS 196.86 KC584522 KC584266 KC584390 FJ266475 AY562401 KC584649
A. conoidea CBS 132.89 KC584585 KC584327 KC584452 AF348226 FJ348227 KC584711
A. consortialis CBS 104.31 KC584615 KC584357 KC584482 KC584247 KC584173 KC584742
A. cucurbitae CBS 483.81 KC584616 KC584358 KC584483 FJ266483 AY562418 KC584743
A. cumini CBS 121329 KC584523 KC584267 KC584391 KC584191 KC584110 KC584650
A. daucifolii CBS 118812 KC584525 KC584269 KC584393 KC584193 KC584112 KC584652
A. dennisii CBS 110533 KC584586 KC584328 KC584453 KC584232 KC584157 KC584712
A. dennisii CBS 476.90 KC584587 KC584329 KC584454 JN383488 JN383469 KC584713
A. dianthicola CBS 116491 KC584526 KC584270 KC584394 KC584194 KC584113 KC584653
A. didymospora CBS 766.79 KC584588 KC584330 KC584455 FJ357312 FJ357300 KC584714
A. elegans CBS 109159 KC584527 KC584271 KC584395 KC584195 KC584114 KC584654
A. embellisia CBS 339.71 KC584582 KC584324 KC584449 KC584230 KC584155 KC584708
A. eryngii CBS 121339 KC584529 KC584273 KC584397 JQ693661 AY562416 KC584656
A.  eureka CBS 193.86 KC584589 KC584331 KC584456 JN383490 JN383471 KC584715
A. geniostomatis CBS 118701 KC584532 KC584276 KC584400 KC584198 KC584117 KC584659
A. gypsophilae CBS 107.41 KC584533 KC584277 KC584401 KC584199 KC584118 KC584660
A. helianthiinficiens CBS 117370 KC584534 KC584278 KC584402 KC584200 KC584119 KC584661
A. helianthiinficiens CBS 208.86 KC584535 KC584279 KC584403 JX101649 KC584120 EU130548
A. heterospora CBS 123376 KC584621 KC584363 KC584488 KC584248 KC584176 KC584748
A. hyacinthi CBS 416.71 KC584590 KC584332 KC584457 KC584233 KC584158 KC584716
A. indefessa CBS 536.83 KC584591 KC584333 KC584458 KC584234 KC584159 KC584717
A. infectoria CBS 210.86 KC584536 KC584280 KC584404 DQ323697 AY278793 KC584662
A.  japonica CBS 118390 KC584537 KC584281 KC584405 KC584201 KC584121 KC584663
A. kulundii M313 KJ443087 KJ443132 KJ443176 KJ443262 KJ649618
A. leucanthemi CBS 421.65 KC584605 KC584347 KC584472 KC584240 KC584164 KC584732
A. leucanthemi CBS 422.65 KC584606 KC584348 KC584473 KC584241 KC584165 KC584733
A. limaciformis CBS 481.81 KC584539 KC584283 KC584407 KC584203 KC584123 KC584665
A. macrospora CBS 117228 KC584542 KC584286 KC584410 KC584204 KC584124 KC584668
A. nepalensis CBS 118700 KC584546 KC584290 KC584414 KC584207 KC584126 KC584672
A. nobilis CBS 116490 KC584547 KC584291 KC584415 KC584208 KC584127 KC584673
A. obclavata CBS 124120 KC584575 FJ839651 KC584443 KC584225 KC584149 KC584701
A. oudemansii CBS 114.07 KC584619 KC584361 KC584486 FJ266488 KC584175 KC584746
A. omaniana SQUCC 13580 MK878559 MK878556 MK880893 MK878562 MK880899 MK880896
A. omaniana SQUCC 15560 MK878560 MK878557 MK880894 MK878563 MK880900 MK880897
A. omaniana SQUCC 15561 MK878561 MK878558 MK880895 MK878564 MK880901 MK880898
A. panax CBS 482.81 KC584549 KC584293 KC584417 KC584209 KC584128 KC584675
A. papavericola CBS 116606 KC584579 KC584321 KC584446 FJ357310 FJ357298 KC584705
A. penicillata CBS 116608 KC584572 KC584316 KC584440 FJ357311 FJ357299 KC584698
A. penicillata CBS 116607 KC584580 KC584322 KC584447 KC584229 KC584153 KC584706
A. perpunctulata CBS 115267 KC584550 KC584294 KC584418 KC584210 KC584129 KC584676
A. petroselini CBS 112.41 KC584551 KC584295 KC584419 KC584211 KC584130 KC584677
A. petuchovskii M304 KJ443079 KJ443124 KJ443170 KJ443254 KJ649616
A. photistica CBS 212.86 KC584552 KC584296 KC584420 KC584212 KC584131 KC584678
A. phragmospora CBS 274.70 KC584595 KC584337 KC584462 JN383493 JN383474 KC584721
A. porri CBS 116698 KC584553 KC584297 KC584421 DQ323700 KC584132 KC584679
A. proteae CBS 475.90 KC584597 KC584339 KC584464 AY278842 KC584161 KC584723
A. pseudorostrata CBS 119411 KC584554 KC584298 KC584422 JN383483 AY562406 KC584680
A. radicina CBS 245.67 KC584555 KC584299 KC584423 KC584213 KC584133 KC584681
A. scirpicola CBS 481.90 KC584602 KC584344 KC584469 KC584237 KC584163 KC584728
A. septorioides CBS 106.41 KC584559 KC584303 KC584427 KC584216 KC584136 KC584685
A. septospora CBS 109.38 KC584620 KC584362 KC584487 FJ266489 FJ266500 KC584747
A. shukurtuzii M307 KJ443082 KJ443127 KJ443172 KJ443257 KJ649620
A. simsimi CBS 115265 KC584560 KC584304 KC584428 JF780937 KC584137 KC584686
A. slovaca CBS 567.66 KC584576 KC584319 KC584444 KC584226 KC584150 KC584702
A. smyrnii CBS 109380 KC584561 KC584305 KC584429 AF229456 KC584138 KC584687
A. solani CBS 116651 KC584562 KC584306 KC584430 KC584217 KC584139 KC584688
A. soliaridae CBS 118387 KC584563 KC584307 KC584431 KC584218 KC584140 KC584689
A. solidaccana CBS 118698 KC584564 KC584308 KC584432 KC584219 KC584141 KC584690
A. sonchi CBS 119675 KC584565 KC584309 KC584433 KC584220 KC584142 KC584691
Alternaria sp. CBS 175.52 KC584577 KC584320 KC584445 KC584227 KC584151 KC584703
A. tagetica CBS 479.81 KC584566 KC584310 KC584434 KC584221 KC584143 KC584692
A. tellustris CBS 538.83 KC584598 KC584340 KC584465 FJ357316 AY562419 KC584724
A. thalictrigena CBS 121712 KC584568 KC584312 KC584436 EU040211 KC584144 KC584694
A. triglochinicola CBS 119676 KC584569 KC584313 KC584437 KC584222 KC584145 KC584695
A. vaccariae CBS 116533 KC584570 KC584314 KC584438 KC584223 KC584146 KC584696
A. vaccariicola CBS 118714 KC584571 KC584315 KC584439 KC584224 KC584147 KC584697

Fig Phylogenetic tree generated by maximum parsimony analysis of combined SSU, LSU, ITS, GPDH, tef1 and RPB2 sequence data of Alternaria species. One hundred strains are included in the analyses, which comprised 4056 characters including gaps. The tree was rooted with Stemyphylium herbarium (CBS 191.86) and Pleospora tarda (CBS 714.68). The maximum parsimonious dataset consisted of 3091 constant, 852 parsimony-informative and 113 parsimony-uninformative characters. The parsimony analysis of the data matrix resulted in the maximum of ten equally most parsimonious trees with a length of 4520 steps (CI = 0.335, RI 0.708, RC = 0.237, HI = 0.665) in the first tree. MP and ML bootstrap values ≥50% and Bayesian posterior probabilities ≥0.90 are shown respectively near the nodes. Ex-type strains are in bold.

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