Mycosphere 12(1): 519–669 (2021) www.mycosphere.org ISSN 2077 7019 Article Doi 10.5943/mycosphere/12/1/7 Colletotrichum: lifestyles, biology, morpho-species, species complexes and accepted species Jayawardena RS1,3, Bhunjun CS1,3, Hyde KD1,2,3,4*, Gentekaki E1,3 and Itthayakorn P2 1Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai, 57100, Thailand 2Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand 3School of Science, Mae Fah Luang University, Chiang Rai, 57100, Thailand 4Innovative Institute of Plant Health, Zhongkai University of Agriculture and Engineering, Haizhu District, Guangzhou 510225, People’s Republic of China Jayawardena RS, Bhunjun CS, Hyde KD, Gentekaki E, Itthayakorn P 2021 – Colletotrichum: lifestyles, biology, morpho-species, species complexes and accepted species. Mycosphere 12(1), 519–669, Doi 10.5943/mycosphere/12/1/7 Abstract Colletotrichum is an important plant pathogenic genus that has undergone tremendous taxonomic changes. Species of Colletotrichum also occur as endophytes, saprobes and rarely entomopathogens. The current understanding of Colletotrichum taxonomy and application of various techniques in defining species within the genus is discussed in this paper. Here we provide a review of lifestyles, infection mechanisms, life cycle, host-specificity, classification history and techniques defining Colletotrichum species and the relation to speciation. Misidentifications and mistakes during species introduction are discussed and recommendations are provided for valid species publication. We provide an account of 248 currently accepted species with molecular data, which falls into 14 species-complexes and 13 singleton species. An updated account of Colletotrichum species is provided. Species are listed alphabetically in each species complex and annotated with their habitat, host, geographic distribution, phylogenetic position and typification details. Tables of host specific (152 species) and geographically endemic Colletotrichum species (19 species) are provided. A table of 450 morpho-species is provided for the first time gathering all data to one place, allowing mycologists to check before publishing a new species. Phylogenetic trees are provided for the whole genus and each species complex. Genes and combinations of genes that can be used for the identification of the species complexes are suggested. Future directions for the advancement of this genus are discussed. Keywords – Host-specificity – Morpho-species – Pathogens – Singleton – Taxonomy Introduction Colletotrichum is the sole member of Glomerellaceae (Glomerellales, Sordariomycetes), and was introduced by Corda (1831) (Réblová et al. 2011, Maharachchikumbura et al. 2015, 2016, Hyde et al. 2020). Many species of this genus are important pathogens, while some are endophytes and saprobes (Cannon et al. 2012, Hyde et al. 2014, 2020, Jayawardena et al. 2016a, 2020). At the time of the first monographic treatment of Colletotrichum (von Arx 1957b), around 750 names existed (Cannon et al. 2012). von Arx (1957b) reduced this to 11 taxa based on morphological characters. Sutton (1980) accepted 22 species, while Sutton (1992) accepted 39 species based on Submitted 16 January 2021, Accepted 29 March 2021, Published 7 May 2021 Corresponding Author: K.D. Hyde – e-mail – [email protected] 519 morphological and cultural characteristics. Misidentification of Colletotrichum species occurs frequently due to only a few distinctive morphological characters being available for identification (Hyde et al. 2009a, Cannon et al. 2012, Jayawardena et al. 2016a). Hyde et al. (2009b) provided the first comprehensive overview of this genus with 66 names in common use and 19 doubtful names and also highlighted the need to revise this genus by using molecular methods (Hyde et al. 2009a). This study laid the foundation for the ongoing polyphasic research approaches on Colletotrichum (Cannon et al. 2012, Damm et al. 2012a, b, 2013, 2014, 2019, Weir et al. 2012, Liu et al. 2014, Jayawardena et al. 2016a, 2020). Here we provide a review of lifestyles, infection mechanisms, life cycle, host-specificity, classification history and techniques for defining Colletotrichum species. We also discuss whether the scientific community has introduced too many species based on examples. This study uses Jayawardena et al. (2016a) as the starting point for accepted species, and also includes published records since that study. An overview of the currently accepted species in the genus along with their hosts, geographic distribution, phylogenetic position and sexual morphs are provided. Updated phylogenetic trees for the whole genus and the species complexes are also provided. When possible, the use of specific gene regions necessary to distinguish the species within the different species complexes is mentioned. Lifestyles Plant pathogenic fungi may have different lifestyles and infection mechanisms to colonise their hosts (Agrios 2005). Lifestyle patterns in Colletotrichum can be broadly categorised as endophytic, hemibiotrophic, necrotrophic, latent or quiescent (Perfect et al. 1999, Peres et al. 2005, Cannon et al. 2012, Barimani et al. 2013, de Silva et al. 2017). Hemibiotrophy is the most common among the above lifestyles (Cannon et al. 2012, Jayawardena et al. 2016a, de Silva et al. 2017). Being a complex genus, Colletotrichum has different lifestyles that vary between groups of species, many of which can switch between lifestyles (Promputtha et al. 2007, O’Connell et al. 2012). Most plant pathogenic taxa can change their relationships with the host at different stages of their life cycle. The physiological maturity and resistance of the hosts, environmental factors and virulence genes of the fungal taxa underpin the change (O’Connell et al. 2012, Stergiopoulos & Gordon 2014). Species of Colletotrichum undergo major transformations in cell morphology and infection mode when switching lifestyles (O’Connell et al. 2012). Specific gene families and biochemical interactions, such as the production of enzymes and secondary metabolites (Gan et al. 2016), regulate the lifestyle patterns of Colletotrichum species. Genomic- and transcriptomic-based research during the past decade has provided valuable insights into the relationship between genetics and lifestyles of Colletotrichum (Gan et al. 2013, 2016, 2019, Zeilinger et al. 2016). These studies have uncovered information on the evolution of lifestyles and their functional relationships and have also identified potential targets for control and management (Crouch et al. 2014). The available genomic data of Colletotrichum species comes from representatives of six independent species complexes (acutatum, destructivum, gloeosporioides, graminicola, orbiculare and spaethianum) and include endophytes, foliar and fruit pathogens (Liang et al. 2018). Comparative analyses of these genomes have revealed that Colletotrichum species may tailor their plant cell wall degrading enzymes and proteinases according to their lifestyle (O’Connell et al. 2012, Baroncelli et al. 2016, Hacquard et al. 2016). These genomes are also recorded to code for enzymes that catalyse the biosynthesis of secondary metabolites and are expressed in a phase-specific fashion (O’Connell et al. 2012). Understanding different lifestyles of Colletotrichum and interactions with their hosts is important for plant biosafety and quarantine purposes (Bourget et al. 2013). However, changes in lifestyle patterns during the life cycle of a Colletotrichum species make detection and control difficult (de Silva et al. 2017). It is important to realize that export/import provide venues for species of Colletotrichum to disperse in asymptomatic plant materials over long distances and may result in the introduction of a completely new disease to a country. Therefore, understanding the lifestyles of this genus is important when considering quarantine measures and world trade 520 (Newton et al. 2010, de Silva et al. 2017). In this section, we review the different lifestyles in Colletotrichum with examples. Biotrophic and hemibiotrophic lifestyles In a biotrophic lifestyle, the pathogen remains inside the living plant tissue and actively absorbs nutrients without killing the plant cells (Mendgen & Hahn 2002). Different strategies to avoid defence responses of the host, such as masking of invading hyphae or active suppression of the defence, are essential for a biotrophic parasitic lifestyle (Münch et al. 2008). Without a biotrophic phase, the initial death of host cells could lead to recognition and initiation of host defence responses that could inhibit fungal growth (Münch et al. 2008). Even though Colletotrichum is not considered a true biotroph, many species do have a biotrophic stage in their life cycle, which is followed by a necrotrophic lifestyle, and is referred to as hemibiotrophic. This strategy may also contribute to the prominence of Colletotrichum species as symptomless endophytes in living plant tissues (Rojas et al. 2010, Cannon et al. 2012). Nascent colonies of many species of Colletotrichum enter a biotrophic phase, while infected tissues remain externally symptomless. This period may be short (1-3 days) or extended (probably dormant) (Prusky & Plumbley 1992, Cannon et al. 2012). When Colletotrichum enters the necrotrophic stage, it results in the death of a significant number of plant cells, which is followed by the emergence of symptoms (Cannon et al. 2012, Jayawardena et al. 2016a). Depending on host development