Cercospora

Cercospora Fresen. ex Fuckel, Hedwigia 2(15): 133 (1863)

Background

Cercospora includes pathogens, saprobes and endophytes. Species are widely distributed, occurring on numerous flowering and ornamental plants, ferns, other fungi (as parasites), gymnosperms, grasses and other monocotyledons such as lilies, magnoliids and palms, mostly causing leaf spots. The well-known asexual morph, which is hyphomycetous, are among the largest groups of plant pathogenic fungi causing leaf spots, leading to diseases on many economically important crops (Agrios 2005; To-Anun et al. 2011; Groenewald et al. 2013; Guatimosim et al 2016; Park et al. 2017). Comparatively only a few sexual morphs have been studied (Hyde et al. 2013). A photosensitizing toxic compound named ‘cercosporin’ is responsible for Cercospora species inhabiting such a wide host range (Daub et al. 2005; Thomas et al. 2020).

Classification – Ascomycota, Dothideomycetes, Dothideomycetidae, Capnodiales, Mycosphaerellaceae

Type species Cercospora apii Fresen., Beitr. Mykol. 3: 91 (1863)

Distribution – Worldwide

Disease symptoms – Leaf blights and spots

This disease affects the leaves, petioles, stems and peduncles of the tree. Infection and lesion formation initially occur on older leaves before progressing to newer ones. Small, brown flecks develop with a reddish border, expanding to circular spots with an ashy-grey centre. Concentric rings may be observed as individual lesions expand. This tissue becomes thin and brittle, and often drops out, leaving a ragged hole. These lesions often resemble frogeyes, giving this disease its common name. Severely affected leaves wither and die from coalescing lesions (Shane and Teng 1992; Steddom et al. 2005).

Species of Cercospora cause blights and spots on the leaves, petioles, stems and peduncles of trees. Often infection and lesion formation occurs on older leaves before progressing to newer ones. Common symptoms include small, brown lesions that develop with a reddish border, eventually expanding to larger circular or angular spots. Concentric rings may be observed as individual lesions expand. The tissue becomes thin and brittle, and often drops out, leaving a ragged hole. Severely affected leaves wither and die from coalescing lesions (Shane and Teng 1992; Steddom et al. 2005).

Hosts – Wide host range including plant genera in Amaranthaceae, Apiaceae, Asteraceae, Arecaceae, Chenopodiaceae, Convolvulaceae, Cryptogammaceae, Cucurbitaceae, Cyatheaceae, Dennstaedtiaceae, Dioscoreaceae, Euphorbiaceae, Fabaceae, Gunneraceae, Hydrangeaceae, Lamiaceae, Lygodiaceae, Musaceae, Myrtaceae, Onagraceae, Plumbaginaceae, Poaceae, Pteridaceae, Scrophulariaceae, Solanaceae, Thelypteridaceae and Urticaceae (Farr and Rossman 2020).

Cercospora apii causes leaf spot disease on celery and C. beticola on sugar beet (Braun et al. 2013; Guatimosim et al. 2016). The pathogen Cercospora cf. sigesbeckiae infects various plant families, including economically valuable crops such as soybean, causing ‘Cercospora leaf blight’, a disease characterized by leaf bronzing (Albu et al. 2016 2017). Some other species identified as causative organisms of the leaf blight are C. kikuchii and C. cf. flagellaris (Soares et al. 2015; Rezende et al. 2020). The yield losses related to Cercospora disease have been reported from Canada, China, India and other regions in the USA and South America (Almeida et al. 2005; Cai et al. 2009; Hershman 2009; Wrather et al. 2010; Geisler et al. 2013; Albu et al. 2017; Bandara et al. 2020). Cercospora is among the leading fungal pathogens that cause a severe threat to soybean, which is an important grain legume crop, by reducing seed production and quality (Arantes et al. 2020). Two notable pathogens on soybean are C. kikuchii (leaf blight and purple seed stain) and C. sojina (frogeye leaf spot) (Soares et al. 2015)

Other notable reports include Cercospora leaf spots, which are the most common and destructive of the Hibiscus diseases, often resulting in complete crop loss (Park et al. 2017) and more than 200 fungal species in association with various diseases of ‘kenaf’ (Hibiscus cannabinus) worldwide (Park et al. 2017). Key proteins and expression of genes that could inhibit the pathogen C. kikuchii in soybean (Arantes et al. 2020) have been investigated. However, based on previous reports, morphological characters, phylogeny and pathogenicity of Cercospora cf. nicotianae was identified as one of several cryptic species causing Cercospora leaf blight (Sautua et al. 2019, 2020). Thomas et al. (2020) proposed the expression of fungal cercosporin auto resistance genes and silencing of the cercosporin pathway as effective strategies to combat Cercospora diseases.

Pathogen biology, disease cycle and epidemiology

The taxa survive on undecomposed residues in soil, on weed hosts and seeds. Leaf spot disease is favoured by warm, wet weather. Severe outbreaks generally require a period of showery weather. Infection from germinating fungal spores occurs via penetration of leaf stomata by fungal hyphae. Spores spread in wind, rain, irrigation or via mechanical tools (Vereijssen 2004; Lin and Kelly 2018).

Morphological based identification and diversity

Cercospora has been widely applied to all kinds of dematiaceous hyphomycetous asexual morphs characterized by holoblastic conidiogenesis and some associated with “Mycosphaerella”-like sexual morphs (Hyde et al. 2013; Groenewald et al. 2013). Species resembling the genus type, C. penicillata, characterized by pigmented conidiophores, thickened and darkened conidiogenous loci and singly formed colourless conidia are identified as Cercospora sensu stricto (Ellis 1971, 1976). Chupp (1954) published a worldwide monograph of this group which listed 1,419 species. A vast number of studies related to Cercospora are based on morphology or confined to specific regions or hosts (Phengsintham et al. 2013a, b). Hence, more than 3,000 species of Cercospora have been described (Pollack 1987), often as a result of taxa being considered as host-specific at a genus or family level (Crous and Braun 2003; Groenewald et al. 2005). However, based on morphological features of the structure of conidiogenous loci and hila, absence or presence of pigmentation in conidiophores and conidia, Crous and Braun (2003) revised the generic circumscription of Cercospora, resulting in the reduction of the number of species to 659. A series of publications related to Cercospora and its allied genera in Mycosphaerellaceae, along with illustrations and descriptions of sexual morphs was published by Braun et al. (2013, 2014, 2015a, b, 2016).

Molecular based identification and diversity

Cercospora is monophyletic (Stewart et al. 1999; Hyde et al. 2013). Groenewald et al. (2013) provided a comprehensive phylogenetic analysis of 360 isolates which included ITS, and protein-coding genes; translation elongation factor 1-alpha (tef1), actin (act), calmodulin (cal) and histone 3 (his). This provided a basis for the identification of Cercospora species, indicating most to be host-specific (Park et al. 2017). Bakhshi et al. (2018) subjected 170 Cercospora isolates to an eight-gene analysis (tef1, act, cal, his, tub2, rpb2, gapdh) which resulted in several new clades within the C. apii, C. armoraciae, C. beticola, C. cf. flagellaris and Cercospora sp. G. complexes. The combination of tef1, cal, tub2, rpb2 and gapdh provided high phylogenetic resolution for distinguishing Cercospora species with gapdh being the gene effective in distinguishing the species complexes (Bakhshi et al. 2018). The genomes for several species – Cercospora arachidicola, C. aff. canescens, C. cf. sigesbeckiae, C. kikuchii, C. sojina and C. zeae-maydis have been published, of which C. cf. sigesbeckiae and C. sojina are important soybean pathogens (Albu et al. 2017; Sautua et al. 2019). The mating-type genes of some asexual Cercospora species have been characterised (Groenewald et al. 2013), of which C. beticola, C. zeaemaydis and C. zeina are heterothallic, while only one mating type was discovered in populations of C. apii and C. apiicola (Groenewald et al. 2006, 2010).

In soybean cultivation regions such as China, Latin America or the USA, C. sojina occurs as several pathotypes named as races, and their existence differs from soybean cultivar-to-cultivar (Athow et al. 1962; Yorinori and Henechin 1978; Mian et al. 2008; Gu et al. 2020). Apart from being differentiated physiologically, several molecular genetic tools such as AFLPs (Amplified Fragment Length Polymorphisms), SSR markers and SNP markers have been utilized to characterize their population diversity (Gu et al. 2020). The combination of DNA sequence data with ecology, morphological and cultural characteristics named as the Consolidated Species Concept (Quaedvlieg et al. 2014) is an effective method for delimiting Cercospora species (Groenewald et al. 2013; Bakhshi et al. 2015a, 2018). Here we provide an updated phylogenetic tree of combined ITS, tef1, act, cal, his, tub2, rpb2 and gapdh (Fig. 1).

Recommended genetic markers (genus level) – LSU, ITS

Recommended genetic markers (species level) – ITS, tef1, act, cal, his, tub2, rpb2, gapdh

Accepted number of species – There are over 3100 epithets listed in Index Fungorum (2020), however, only 134 have DNA sequence data (Table 1).

References – Braun et al. 2013, 2014, 2015a, b, 2016 (morphology), Groenewald et al. 2013 (morphology, phylogeny), Albu et al. 2017 (morphology, phylogeny), Guatimosim et al. 2016 (morphology, phylogeny), Bakhshi et al. 2015a, 2018 (morphology, phylogeny).

Table 1 DNA barcodes available for Cercospora. Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher strains are also in bold. Species confirmed with pathogenicity studies are marked with #.

Species Isolate no ITS tef1 act cal his tub2 rpb2 gapdh
Cercospora achyranthis CBS 132613 JX143523 JX143277 JX143031 JX142785 JX142539
  CPC 10091 JX143524 JX143278 JX143032 JX142786 JX142540
C. agavicola# CBS 117292* AY647237 AY966897 AY966898 AY966899 AY966900
C. alchemillicola# CPC 5259* JX143525 JX143279 JX143033 JX142787 JX142541
C. althaeina CBS 248.67* JX143530 JX143284 JX143038 JX142792 JX142546 MH496340 MH496170
C. apii# CBS 116455* AY840519 AY840486 AY840450 AY840417 AY840384 MH496343 MH496173
C. apiicola# CBS 116457* AY840536 AY840503 AY840467 AY840434 AY840401
C. armoraciae# CBS 250.67* JX143545 JX143299 JX143053 JX142807 JX142561 MH496351 MH496181
C. beticola# CBS 116456* AY840527 AY840494 AY840458 AY840425 AY840392 MH496355 KT216555 MH496185
C. bizzozeriana# CBS 258.67* JX143546 JX143300 JX143054 JX142808 JX142562 MH496368 MH496198
C. cf. brunkii CBS 132657 JX143559 JX143313 JX143067 JX142821 JX142575
C. campi-silii CBS 132625 JX143561 JX143315 JX143069 JX142823 JX142577
C. canescens# CPC 15871 JX143567 JX143321 JX143075 JX142829 JX142583
  CBS 111133 AY260065 DQ835084 DQ835103 DQ835130 DQ835157
C. capsici# CBS 132622 JX143568 JX143323 JX143077 JX142831 JX142585
C. celosiae CBS 132600 JX143570 JX143326 JX143080 JX142834
C. chenopodii# CBS 132594* JX143572 JX143328 JX143082 JX142836 JX142590
CCTU 1060 KJ886438 KJ886277 KJ885955 KJ885794 KJ886116 MH496371 MH511862 MH496201
C. chinensis CBS 132612 JX143578 JX143334 JX143088 JX142842 JX142596
C. citrullina# CBS 119395 EU514222 JX143335 JX143089 JX142843
  MUCC 576 JX143579 JX143337 JX143091 JX142845
C. coniogrammes CBS 132634* JX143583 JX143341 JX143095 JX142849 JX142603
C. convolvulicola CCTU 1083* KJ886441 KJ886280 KJ885958 KJ885797 KJ886119 MH496374 MH511865 MH496204
C. conyzae-canadensis CCTU 1119* KJ886445 KJ886284 KJ885962 KJ885801 KJ886123 MH496377 MH511868 MH496207
C. corchori MUCC 585* JX143584 JX143342 JX143096 JX142850 JX142604
C. cf. coreopsidis CBS 132598 JX143585 JX143343 JX143097 JX142851 JX142605
C. cylindracea CCTU 1081* KJ886449 KJ886288 KJ885966 KJ885805 KJ886127 MH496381 MH511872 MH496211
C. delaireae CBS 13259* JX143587 JX143345 JX143099 JX142853 JX142607
C. dianellicola CBS 143453* MG386075 MG674152 MG674153
C. dispori CBS 13260* JX143591 JX143349 JX143103 JX142857 JX142611
C. cf. erysimi CBS 115059 JX143592 JX143350 JX143350 JX142858 JX142612
C. euphorbiaesieboldianae CBS 113306* JX143593 JX143351 JX143105 JX142859 JX142613
C. fagopyri CBS 132623* JX143594 JX143352 JX143106 JX142860 JX142614
C. cf. nicotianae CBS 131.32 DQ835073 DQ835099 DQ835119 DQ835146
  CBS 132632 JX143631 JX143631 JX143144 JX142898
C. cf. flagellaris# CCTU 1159 KJ886493 KJ886332 KJ886010 KJ885849 KJ886171 MH496388 MH511879 MH496218
  CBS 132653 JX143603 JX143361 JX143115 JX142869 JX142623 MH496390 MH511881 MH496220
  CCTU 1204 KJ886505 KJ886344 KJ886022 KJ885861 KJ886183 MH496399 MH511890 MH496229
  CBS 132667 JX143604 JX143362 JX143116 JX142870 JX142624 MH496401 MH511892 MH496231
  CCTU 1172 KJ886501 KJ886340 KJ886018 KJ885857 KJ886179 MH496409 MH511900 MH496239
  CCTU 1154 KJ886489 KJ886328 KJ886006 KJ885845 KJ886167 MH496410 MH511901 MH496240
C. gamsiana CCTU 1074* KJ886426 KJ886265 KJ885943 KJ885782 KJ886104 MH496446 MH511937 MH496276
C. cf. gossypii CCTU 1070 KJ886467 KJ886306 KJ885984 KJ885823 KJ886145 MH496452 MH511943 MH496282
C. helianthicola# MUCC 716 JX143615 JX143374 JX143128 JX142882 JX142636
C. ipomoeae# CBS 132639 JX143616 JX143375 JX143129 JX142883 JX142637
C. iranica CCTU 1137* KJ886513 KJ886352 KJ886030 KJ885869 KJ886191 MH496455 MH511946 MH496285
C. kikuchii CBS 128.27* DQ835070 DQ835088 DQ835107 DQ835134 DQ835161
C. lactucae-sativae CBS 132604 JX143621 JX143380 JX143134 JX142888 JX142642
C. malayensis KUS-F27687 KR400012 KY082663 KY082664 KY082665 KY082666
C. cf. malloti MUCC 575 JX143625 JX143384 JX143138 JX142892 JX142646
C. mercurialis CBS 550.71* JX143628 JX143628 JX143141 JX142895 JX142649
C. cf. modiolae CPC 5115 JX143630 JX143389 JX143143 JXJX142897 JX142651
C. cf. nicotianae CBS 131.32 DQ835073 DQ835099 DQ835119 DQ835146 DQ835173
  CBS 132632 JX143631 JX143390 JX143144 JX142898 JX142652
C. olivascens CBS 253.67* JX143632 JX143391 JX143145 JX142899 JX142653
C. cf. physalidis# CBS 765.79 JX143633 JX143392 JX143146 JX142900
C. pileicola CBS 132607* JX143634 JX143393 JX143147 JX142901 JX142655
C. plantaginis CBS 252.67* DQ233318 DQ233342 DQ233368 DQ233394 DQ233420 MH496461 MH496291
C. polygonacea CBS 132614 JX143637 JX143396 JX143150 JX142904 JX142658
C. pseudochenopodii CBS 136022* KJ886516 KJ886355 KJ886033 KJ885872 KJ886194 MH496464 MH511954 MH496294
C. punctiformis CBS 132626 JX143638 JX143397 JX143151 JX142905 JX142659
C. cf. resedae CBS 118793 JX143639 JX143398 JX143152 JX142906 JX142660
C. cf. richardiicola# CBS 132627 JX143640 JX143399 JX143153 JX142907 JX142661 MH496465 MH511955 MH496295
C. ricinella# CBS 132605 JX143646 JX143405 JX143159 JX142913 JX142667
C. rodmanii CBS 113123 DQ835076 AF146136 DQ835122 DQ835149 DQ835176
C. rumicis CCTU 1123 KJ886521 KJ886360 KJ886038 KJ885877 KJ886199 MH496466 MH511956 MH496296
C. rumicis CPC 5439 JX143648 JX143407 JX143161 JX142915 JX142669
C. samambaiae CPC 24673 KT037514 KT037474 KT037596 KT037463 KT037555
C. senecioniswalkeri CBS 132636 JX143649 JX143408 JX143162 JX142916 JX142670
C. cf. sigesbeckiae# CBS 132675 JX143655 JX143414 JX143168 JX142922 JX142676
C. sojina CBS 132615 JX143659 JX143419 JX143173 JX142927 JX142681
C. solani# CCTU 1043 KJ886523 KJ886362 KJ886040 KJ885879 KJ886201 MH496469 MH511959 MH496299
C. sorghicola CCTU 1173* KJ886525 KJ886364 KJ886042 KJ885881 KJ886203 MH496471 MH511961 MH496301
Cercospora sp. P CBS 116365* AY752141 AY752176 AY752204 AY752235 AY752266
Cercospora sp. P JZG-2013 JX143714 JX143473 JX143227 JX142981 JX142735
Cercospora sp. G CCTU 1197 KJ886540 KJ886379 KJ886057 KJ885896 KJ886218 MH496472 MH511962 MH496302
Cercospora sp. G CCTU 1015 KJ886528 KJ886367 KJ886045 KJ885884 KJ886206 MH496473 MH511963 MH496303
Cercospora sp. G CCTU 1090 KJ886536 KJ886375 KJ886053 KJ885892 KJ886214 MH496476 MH511965 MH496306
Cercospora sp. G CBS 115518 JX143681 JX143441 JX143195 JX142949 JX142703 MH496480 MH496310
Cercospora sp. T CCTU 1148 KJ886541 KJ886380 KJ886058 KJ885897 KJ886219 MH496488 MH511976 MH496318
C. uwebaruniana CCTU 1200* KJ886408 KJ886247 KJ885925 KJ885764 KJ886086 MH496489 MH511977 MH496319
C. vignigena CBS 132611* JX143734 JX143493 JX143247 JX143001 JX142755
C. violae# CBS 251.67* JX143737 JX143496 JX143250 JX143004 JX142758 MH496492 MH496322
C. zeae-maydis# CBS 117757* DQ185074 DQ185086 DQ185098 DQ185110 DQ185122
C. zebrina# CCTU 1225 KJ886550 KJ886389 KJ886067 KJ885906 KJ886228 MH496495 MH511981 MH496325
  CCTU 1239 KJ886551 KJ886390 KJ886068 KJ885907 KJ886229 MH496504 MH511987 MH496334
C. zeina# CBS 118820* DQ185081 DQ185093 DQ185105 DQ185117 DQ185129
C. cf. zinniae CBS 132624 JX143756 JX143518 JX143272 JX143026
  CCTU 1003 KJ886552 KJ886391 KJ886069 KJ885908 KJ886230 MH496505 MH511988 MH496335

Fig. 1 The most parsimonious tree generated by MP analysis of combined ITS, tef1, act, cal, his, tub2, rpb2 and gapdh sequence data of Cercospora species is presented. Related sequences were obtained from previous publications and GenBank. Eighty-eight strains are included in the analysis comprising 4242 characters including gaps, of which 3044 characters are constant, 464 characters are parsimony-uninformative and 734 are parsimony-informative. The parsimony analysis of the data matrix resulted in the maximum of 84 equally most parsimonious trees with a length of 2886 steps (CI = 0.556, RI=0.700, RC = 0.389, HI = 0.444) in the first tree. The tree was rooted with Septoria provencialis (CPC 12226). Tree topology of the MP analysis was similar to the ML and BYPP analyses. ML and MP bootstrap support value ≥70% and BYPP ≥0.95 (ML/ MP/ BYPP) are shown respectively near the nodes. Ex-type strains are in bold.

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