Golovinomyces (U. Braun) V.P. Heluta, Biol. Zh. Armenii 41: 357 (1988)


Braun (1978) introduced Golovinomyces as a section of Erysiphe sensu lato and Heluta (1988a) raised it to genus rank. Braun (1999) and Braun and Takamatsu (2000) accepted Golovinomyces as a distinct genus and established a new tribe, Golovinomyceteae. This is a strictly herb-parasitic genus in the Erysiphaceae. Host-parasite co-speciation was reported between Golovinomyces and Asteraceae hosts using molecular phylogenetic analyses (Matsuda and Takamatsu 2003). It was suggested that Golovinomyces first acquired parasitism on Asteraceae and then diverged to the host tribes Astereae, Cardueae, Heliantheae and Lactuceae. Bremer (1994) pointed out that Golovinomyces may have originated in South America and the geographic distribution expanded into the Northern Hemisphere. However, Takamatsu et al. (2006) suggest that Golovinomyces originated in the Northern Hemisphere, and not in South America. Fabro et al. (2008) profiled genome-wide expression on haustorium formation of G. cichoracearum in Arabidopsis. Research to understand pathogenesis towards plants has been undertaken. A draft whole genome of G. magnicellulatus, the causal agent of phlox powdery mildew was provided by Farinas et al. (2019). McKernan et al. (2020) identified 82 genes associated with resistance to G. chicoracearum, the causal agent of powdery mildew in cannabis.

Classification – Ascomycota, Pezizomycotina, Leotiomycetes, Leotiomycetidae, Erysiphales, Erysiphaceae

Type species Golovinomyces cichoracearum (DC.) V.P. Heluta

Distribution – Worldwide (Mainly in northern hemisphere)

Disease symptoms – powdery mildew

Hosts – Has a wide range of hosts including Asteraceae, Boraginaceae, Cucurbitaceae, Malvaceae, Fabaceae, Lamiaceae, Polygonaceae, Scrophulariaceae, Solanaceae and Verbenaceae.


Pathogen biology, disease cycle and epidemiology

Discussed under Erysiphaceae.

Morphological based identification and diversity

      Golovinomyces is characterized by chasmothecia with mycelioid appendages, several, mostly 2-spored asci, an asexual morph with catenescent conidia that lack fibrosin bodies, and mostly nipple-shaped appressoria (Braun 1978; Qiu et al. 2020a). Heluta (1988a) reallocated Erysiphae cichoracearum to Golovinomyces and now nearly all species of E. cichoracearum are assigned to Golovinomyces. Braun (1987) confined E. cichoracearum to powdery mildews on hosts of Asteraceae and assigned specimens on hosts belonging to other plant families to Erysiphe orontii. Braun and Cook (2012) split G. cichoracearum into several species based on molecular analyses of this complex which suggested a co-evolutionary relationship between Golovinomyces species and tribes of Asteraceae (Matsuda and Takamatsu 2003). Golovinomyces cynoglossi sensu lato, a complex of morphologically similar powdery mildews on the plant family Boraginaceae, was reassessed by Braun et al. (2018) and split into G. asperifoliorum, G. asperifolii and G. cynoglossi based on sequence analyses, biological aspects and morphological differences. Braun et al. (2019) revisited G. orontii and Qiu et al. (2020b) epitypfied and confirmed Erysiphe cucurbitacearum was a synonym of G. tabaci.


Molecular based identification and diversity

A comprehensive phylogenetic analysis by Takamatsu et al. (2013) resulted in a polyphyletic complex that split into three genetically distinct clades. Golovinomyces ambrosiae and G. spadiceus were considered as separate species by Braun and Cook (2012). However, phylogenetic analyses of ITS and 28S rDNA sequences by Takamatsu et al. (2013), including Golovinomyces species on Asteraceae, found that these two species that occur on Asian species of Eupatorium and a multitude of other hosts, including those on other plant families, formed a single large, unresolved clade (lineage III in Takamatsu et al. (2013)). The taxonomic interpretation posed a serious problem as G. ambrosiae and G. spadiceus were treated as two morphologically differentiated species. Hence, the resolution based only on ITS sequence data was considered insufficient to distinguish closely allied species. Most subsequent authors followed the taxonomic treatments in Braun and Cook (2012) and recognized G. ambrosiae and G. spadiceus as separate species, within lineage III, based on morphological differences (Qiu et al. 2020a). However, there is minimal multi loci data for the powdery mildews currently available. Most of the research involves the intra-specific genetic diversity in species such as Blumeria graminis (Walker et al. 2011), Erysiphe necator (Oliveira et al. 2015), Golovinomyces orontii (Pirondi et al. 2015a) and Podosphaera xanthii (Pirondi et al. 2015b). Based on ITS and D1/D2 domain of 28S sequence data, Braun et al. (2019) introduced G. bolayi and G. vincae. Nayak and Bandamaravuri (2019) developed species-specific PCR primers CgF2 and CgR2 for G. orontii (the causal agent of powdery mildew in cucurbits), based on partial ITS and 5.8S rDNA, which resulted in a 233bp fragment of G. orontii.

Recommended genetic markers (genus level) – ITS, LSU

Recommended genetic markers (species level) – Comprehensive applications of multi loci approaches to solve complex taxonomic-phylogenetic problems connected with the species level classification of the powdery mildews are lacking. The phylogenetic analyses of multi loci sequence data, including ITS and LSU, IGS, tub2, chs, and consideration of morphological characters resolve species delimitation in a heterogeneous complex within Golovinomyces.

Accepted number of species – There are 81 epithets listed in Index Fungorum (2020), however, only 41 have molecular data (Table 1, Fig. 1).

References – Braun 1978, 1987, Heluta 1988 (morphology); Braun and Cook 2012, Takamatsu et al. 2013, Braun et al. 2019, Qiu et al. 2020a,b (morphology and phylogeny).

Table 1 DNA barcodes for accepted species of Golovinomyces. 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 Strain no ITS LSU
Golovinomyces adenophorae MUMH<JPN_144 LC516963 AB077632
G. ambrosiae# MUMH345 AB077642 AB077641
G. arabidis HMNWAFU-CF2009256 KR048081 KR048149
G. artemisiae# MUMH175 AB077637 AB077636
G. asperifolii KUS-F24884 MH189697 MH189696
G. asperifoliorum MUMH769 AB077684 AB077684
G. asterum# MUMH941 AB769417 AB769418
G. biocellatus# MUMH4293 AB307671 AB307671
G. bolayi# OLM 35939* LC417106
G. calceolariae MUMH 1934 AB430810 AB430810
G. chrysanthemi MUMH853 AB077654 AB077653
G. cichoracearum# MUMH623 AB077660 AB077660
G. circumfusus# GLM49501 MK452630 MK452703
G. cucubitarum HMJAU-PM91761 MK937796 MK937801
G. cynoglossi# VPRI20429 AB769455
G. depressus MUMH696 AB077675 AB077676
G. echinopis MUMH1363 AB769414
G. euphorbiicola MUMH3807 AB769460
G. fischeri MUMH1345 AB769451 AB769452
G. glandulariae BRIP 70490* NR_166303 MN539541
G. hyoscyami HMNWAFU-CF2013114 KR048155 KR048155
G. inulae MUMH1334 AB769428
G. leuceriae MUMH2527 AB246766
G. longipes# MUMH2489 AB769440
G. macrocarpus HAL 3153* NR_154105
G. magnicellulatus# MUMH441* AB077647 AB077646
G. monardae# MUMH936 AB307668 AB077691
G. montagnei MUMH1082 AB769413
G. neosalviae# MUMH4294 AB307673
G. ocimi MUMH<JPN_:1803 LC306656
G. orontii# G:00295968 LC417099
G. riedlianus HMNWAFU-CF2012033 KR048088 KR048157
G. reginae BCRU4645 AB246759
G. salviae MUMH935 AB769437 AB077690
G. sonchicola# MUMH683 AB077673 AB077672
G. sordidus# MUMHn41 AB077658 AB077657
G. spadiceus# MUMH<JPN_:3708 LC306664
G. tabaci BP-1TOB AF229013 AB022412
G. valerianae HMNWAFU-CF2011034 KR048090 KR048159
G. verbasci# MUMH958 AB769468 AB769469
G. vincae MUMH2480 AB769444

Fig 1 Phylogram generated from MP analysis based on combined sequences of ITS and LSU sequences of all species of Golovinomyces with molecular data. Related sequences were obtained from GenBank. Fourty-two taxa are included in the analyses, which comprise 1401characters including gaps, of which 848 characters are constant, 392 characters are parsimony-uninformative and 161 characters parsimony-informative. The parsimony analysis of the data matrix resulted in the maximum of ten equally most parsimonious trees with a length of 927 steps (CI = 0.740, RI=0.699, RC = 0.517, HI = 0.260) in the second tree. The tree was rooted with Neoerysiphe galeopsidis (MUMH 4680). MP bootstrap support value ≥50% and BYPP ≥0.9 are shown respectively near the nodes. Ex-type strains are in bold.

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