Advances in fungi' classifications in 2007-2020

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Introduction

The living organisms now are distributed on seven kingdoms: Animalia, Archaea, Bacteria, Chromista, Fungi, Plantae, and Protozoa (Ruggiero et al., 2015). The viruses which lay on the margin between living and non-living nature are singled out in the eighth kingdom Viruses by systematics of https://www.catalogueoflife.org/.

Fungi and fungus-like organisms are the largest in number and the most diverse group of causal agents of crops. By the end of the XX century, all of them were part of the kingdom Fungi. Particularly in Ukraine, phytopathologists used fungi systematics by Takhtadzhian (Takhtadzhian, 1991). By this systematics, the kingdom Fungi was consisted from two phyla – Myxomycota (or slime mold) and Mycota (or true fungi). Phylum Mycota was divided into three classes of lower fungi (Chytridiomycetes, Oomycetes, Zygomycetes) and three classes of higher fungi (Ascomycetes, Basidiomycetes, Deuteromycetes).

In the last two decades in fungi systematics, many significant changes were carried out. It was caused by molecular biology active progress, which allows detecting relationships among different organisms groups and using electron microscopy and biochemistry (Karatygin, 1999). Thus now there are many new systems of organisms‟ classifications and in particular, systematics of fungi and fungus-like organisms (Hawksworth et al., 1995; Margulis & Schwartz, 1997; Kusakin & Drozdov, 1994, 1998). As a result, fungi belonging to the one kingdom Fungi belonged to the three kingdoms of nature – Fungi, Protozoa, and Chromista (Hawksworth et al., 1995).

Differentiation of fungi species was based on morphology, physiology, trophic specialization, and mating ability. Sequencing of DNA regions and further studying of phylogeny changed the approach to fungi systematics. According to the existing species concept based on the International Commission on the Taxonomy of Fungi, currently fungi species delineate by phenotypic characters, ecological, morphological, and physiological features, molecular markers, and extrolite profiling (for some species) according to existing species concept based on International Commission on the Taxonomy of Fungi and International Code of Botanical Nomenclature (Sharma et al., 2015).

Different scientific names for anamorph and teleomorph stages of pleomorphic fungi have confused their classification and systematics. Double name in fungi systematics (“one fungus – two names”) was changed in July 2011 during XVIII International Botanical Congress in Melbourne (Melbourne Code 2011 – “one fungus – one name”). However, when one anamorph may associate with more than one genus of the teleomorph stage, the difficulties still exist (Sharma et al., 2015).

Discussion

During the last fifteen years, the kingdom Fungi included from seven phyla (Hibbett et al., 2007) to eighteen phyla (Tedersoo et al., 2018) and even nineteen phyla (Wijayawardene et al., 2020). During this time, many types of research of fungi taxonomy, classification, systematics, and phylogeny was carried out (James et al., 2006; Kirk et al., 2008, 2013; Zhang et al., 2009; Gryganskyi et al., 2012; Wijayawardene et al., 2012, 2017, 2018a, 2018b; Hyde et al., 2013; Phillips et al., 2013; Slippers et al., 2013; Woudenberg et al., 2013; Manamgoda et al., 2014; Phookamsak et al., 2014; Ariyawansa et al., 2015; Jaklitsch et al., 2016; Li et al., 2016; Spatafora et al., 2016; Marin-Felix et al., 2017, 2019; Videira et al., 2017; Valenzuela-Lopez et al., 2018; Voglmayr et al., 2019). This direction of science was and still now an item of different projects for scientists in the world.

Hence by classification of Hibbett et al. (2007) Fungi include one subkingdom Dikaria and phyla: Ascomycota, Basidiomycota, Blastocladiomycota, Chytridiomycota, Glomeromycota, Microsporidia, Neocallimastigomycota that was based on molecular phylogenetic analyses (Table 1). Besides, Hibbett‟s classification includes four subphyla incertae sedis (phylum not assigned): Mucoromycotina, Entomophthoromycotina, Zoopagomycotina, Kickxellomycotina. The total number of classes is thirty-one.

Table 1. The high-level classification of the kingdom Fungi (by Hibbett et al., 2007).

Eleven years later Tedersoo et al. (2018) proposed a classification of the kingdom Fungi, consisting of nine subkingdoms, eighteen phyla, and seventy-six classes (Table 2). Five subkingdoms consist of only one phylum: Aphelidiomyceta – Aphelidiomycota, Blastocladiomyceta – Blastocladiomycota, Basidiobolomyceta – Basidiobolomycota, Olpidiomyceta – Olpidiomycota, Rozellomyceta – Rozellomycota, and one subphylum (appropriate name with suffix -mycotina). The subkingdom Chytridiomyceta includes three phyla: Chytridiomycota with nine classes, Monoblepharomycota with three classes, and Neocallimastigomycota with one class. The subkingdom Zoopagomyceta includes three phyla Entomophthoromycota with two classes, Kickxellomycota with six classes, and Zoopagomycota with one appropriate class. The subkingdom Mucoromyceta includes four phyla: Calcarisporiellomycota with one class, Glomeromycota with three classes, Mortierellomycota with one class, and Mucoromycota with three classes. The subkingdom Dikarya except for phyla Ascomycota and Basidiomycota include the new phylum Entorrhizomycota, which proposed Bauer et al. (2015) as the sister group to other Dikarya.

Table 2. The high-level taxonomy of the kingdom Fungi (by Tedersoo et al., 2018).

In the classification of Tedersoo et al. (2018) every phylum subdivides into one or more subphyla. Dikarya phylum Ascomycota consists of three subphyla: Pezizomycotina with fourteen classes, Taphrinomycotina with five classes, and Saccharomycotina with one class. Phylum Basidiomycota includes four subphyla: Agaricomycotina with three classes, Pucciniomycotina with ten classes, Ustilaginomycotina with four classes, and Wallemiomycotina (which in Hibbett et al. classification (2007) was in status Basidiomycota incertae sedis class) with two classes.

Wijayawardene et al. (2020) proposed Fungi classification agreeing with Tedersoo et al. (2018). In this classification, basal clades consist of sixteen phyla, and higher fungi (Dikarya) are represented by three phyla (Table 3). The difference between Tedersoo et al. (2018) and Wijayawardene et al. (2020) high-level Fungi classification is phylum Caulochytriomycota with one class Caulochytriomycetes in the last classification. This phylum was introduced by Doweld (2014). Also, Wijayawardene et al. (2018, 2020) did not propose such taxonomy rank as subkingdom, and subphylum was proposed only for phyla Calcarisporiellomycota, Entomophthoromycota, Mortierellomycota, Mucoromycota with only one appropriate subphylum (with suffix -mycotina) and for phyla Ascomycota and Basidiomycota (three and four subphyla respectively).

Table 3. The high-level classification of the basal clades and the higher fungi (Wijayawardene et al., 2020).

On the class-level of Wijayawardene et al. (2020) classification, changes were provided in phylum Rozellomycota. To this phylum was included the class Rudimicrosporea in addition to the class Microsporidea. Order Metchnikovellida was placed in the class Rudimicrosporea.

The changes were provided in phyla Basidiomycota and Ascomycota. In the phylum Basidiomycota class Bartheletiomycetes was added to subphylum Agaricomycotina. This class was proposed by research results of Mishra et al. (2018) in Research News (2018) for a single species Bartheletia paradoxa which is associated with Gingko biloba as a “living fossil”. Moreover, now subphylum Agaricomycotina consists of four classes (Agaricomycetes, Bartheletiomycetes, Dacrymycetes, Tremellomycetes).

The class Collemopsidiomycetes proposed in the subphylum Pezizomycotina (phylum Ascomycota) by Tedersoo et al. (2018) was excluded. The single order Collemopsidiales was placed in the class Dothideomycetes. Two new classes of phylum Ascomycota (Candelariomycetes and Xylobotryomycetes), which was proposed by Voglmayr et al. (2019) in the last classification (Wijayawardene et al., 2020) were included in the subphylum Pezizomycotina.

One more change in the high-level classification of Fungi (Wijayawardene et al., 2020) was in excluding class Geminibasidiomycetes with one order Geminibasidiales from subphylum Wallemiomycotina. This class was proposed by Nguyen et al. (2015) for order Geminibasidiales and was including in classification by Tedersoo et al. (2018). In the last classification (Wijayawardene et al., 2020), Geminibasidiales is placed in the single subphylum Wallemiomycotina class Wallemiomycetes.

Despite rapidity and the enormous amount of research in fungi classification and phylogeny significant amount of genera, families, and orders remain in status “incertae sedis” in Wijayawardene et al. (2020). In particular, in the phylum Ascomycota remain not assigned family for 534 genera; not assigned order for 449 genera and 82 families; not assigned class for 1485 genera, for 8 families and 2 orders. In the phylum Basidiomycota remain not assigned family for 342 genera; not assigned order for 61 genera and 4 families and not assigned class for 11 genera. In the phylum Blastocladiomycota remains not assigned family for 1 genus and not assigned order for 1 genus. In the phylum Chytridiomycota remain unassigned family for 7 genera; not assigned order for 39 genera and 5 families; not assigned class for 3 genera. In the phylum Kickxellomycota remain not assigned family for 3 genera. In the phylum Mucoromycota remains not assigned class for 1 genus. In the phylum Rozellomycota remain not assigned family for 24 genera; not assigned class and order for 3 families and not assigned class for 5 genera. In the phylum Zoopagomycota remains not assigned family for 1 genus.

Conclusion

Researches in fungi classification and phylogeny are an amount and significant for understanding relationships between species. In recent decades we have many changes in the systematics and classification of microorganisms. Despite the progress in fungi classification last several decades, many unclarified positions in systematic are remaining. Rapid progress in scientific development allows supposing revisions and improvements of fungi‟s classification in a short time.

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