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Colletotrichum and Pyricularia are destructive fungal phytopathogens that typically invade plants by forming a heavily melanised, unicellular infection structure known as an appressorium, enabling melanised appressorium-mediated entry (MAE). Appressorial melanisation is essential for invasion by these phytopathogens. Here, we report Colletotrichum fungi that can invade plants via nonmelanised appressorium-mediated entry (NMAE). Multifaceted analyses revealed interspecific variation in the degree of melanisation dependence across appressorial functions. NMAE-type appressoria accomplished these functions regardless of melanisation, thus being capable of early invasion. Comprehensive screening identified a monophyletic NMAE-type Colletotrichum group with rapid expansion. Critically, we identified an eccentric NMAE-type strain with erratic appressorial melanisation. We also rediscovered appressorium-independent hyphal tip-based entry (HTE)-type strains. Collectively, these findings establish a key paradigm for the plant infection strategy of Colletotrichum fungi. In contrast to the widely accepted view based on the MAE of Colletotrichum , this study suggests that appressorial melanisation is not universally required, underscoring the need to consider the emergence of NMAE- and HTE-type pathogens. Melanised appressorium-dependent invasion of phytopathogenic anthracnose and rice blast fungi is a longstanding dogma in plant pathology. Here the authors report melanisation- and/or appressorium-independent invasion strategies of anthracnose fungi.

Background Accurate delimitation of plant pathogenic fungi is critical for the establishment of quarantine regulations, screening for genetic resistance to plant pathogens, and the study of ecosystem function. Concatenation analysis of multi-locus DNA sequence data represents a powerful and commonly used approach to recognizing evolutionary independent lineages in fungi. It is however possible to mask the discordance between individual gene trees, thus the speciation events might be erroneously estimated if one simply recognizes well supported clades as distinct species without implementing a careful examination of species boundary. To investigate this phenomenon, we studied Colletotrichum siamense s. lat., which is a cosmopolitan pathogen causing serious diseases on many economically important plant hosts. Presently there are significant disagreements among mycologists as to what constitutes a species in C. siamense s. lat., with the number of accepted species ranging from one to seven. Results In this study, multiple approaches were used to test the null hypothesis “ C. siamense is a species complex”, using a global strain collection. Results of molecular analyses based on the Genealogical Concordance Phylogenetic Species Recognition (GCPSR) and coalescent methods (e.g. Generalized Mixed Yule-coalescent and Poisson Tree Processes) do not support the recognition of any independent evolutionary lineages within C. siamense s. lat. as distinct species, thus rejecting the null hypothesis. This conclusion is reinforced by the recognition of genetic recombination, cross fertility, and the comparison of ecological and morphological characters. Our results indicate that reproductive isolation, geographic and host plant barriers to gene flow are absent in C. siamense s. lat. Conclusions This discovery emphasized the importance of a polyphasic approach when describing novel species in morphologically conserved genera of plant pathogenic fungi.

Hemibiotrophic fungal plant pathogens represent a group of agronomically significant disease‐causing agents that grow first on living tissue and then cause host death in later, necrotrophic growth. Among these, Colletotrichum spp. are devastating pathogens of many crops. Identifying expanded classes of genes in the genomes of phytopathogenic Colletotrichum, especially those associated with specific stages of hemibiotrophy, can provide insights on how these pathogens infect a large number of hosts. The genomes of Colletotrichum orbiculare, which infects cucurbits and Nicotiana benthamiana, and C. gloeosporioides, which infects a wide range of crops, were sequenced and analyzed, focusing on features with potential roles in pathogenicity. Regulation of C. orbiculare gene expression was investigated during infection of N. benthamiana using a custom microarray. Genes expanded in both genomes compared to other fungi included sequences encoding small, secreted proteins (SSPs), secondary metabolite synthesis genes, proteases and carbohydrate‐degrading enzymes. Many SSP and secondary metabolite synthesis genes were upregulated during initial stages of host colonization, whereas the necrotrophic stage of growth is characterized by upregulation of sequences encoding degradative enzymes. Hemibiotrophy in C. orbiculare is characterized by distinct stage‐specific gene expression profiles of expanded classes of potential pathogenicity genes.

Control of fungal phytopathogens is a significant challenge in modern agriculture. The widespread use of chemical fungicides to control these pathogens often leads to environmental and food contamination. An eco-friendly alternative that can help reduce reliance on these chemicals is plant growth–promoting bacteria (PGPB), particularly those of the genus Paenibacillus , which appear to be highly effective. The review aims to summarize the existing knowledge on the potential of Paenibacillus spp. as fungal biocontrol agents, identify knowledge gaps, and answer whether other species of the genus Paenibacillus , in addition to Paenibacillus polymyxa , can also be effective biocontrol agents. Paenibacillus spp. can combat plant phytopathogens through various mechanisms, including the production of lipopeptides (such as fusaricidin, paenimyxin, and pelgipeptin), the induction of systemic resistance (ISR), hydrolytic enzymes (chitinase, cellulase, and glucanase), and volatile organic compounds. These properties enable Paenibacillus strains to suppress the growth of fungi such as Fusarium oxysporum , F. solani , Rhizoctonia solani , Botrytis cinerea , or Colletotrichum gloeosporioides . Notably, several strains of Paenibacillus , including P. polymyxa , P. illinoisensis KJA-424, P. lentimorbus B-30488, and P. elgii JCK1400, have demonstrated efficacy in controlling fungal diseases in plants. Importantly, many formulations with Paenibacillus strains have already been patented, and some are commercially available, but most of them contain only P. polymyxa . Nevertheless, considering the data presented in this review, we believe that other strains from the Paenibacillus genus (besides P. polymyxa ) will also be commercialized and used in plant protection in the future. Importantly, there is still limited information regarding their impact on the native microbiota, particularly from the metataxonomic and metagenomic perspectives. Expanding knowledge in this area could enhance the effectiveness of biocontrol agents containing Paenibacillus spp., ensuring safe and sustainable use of biological fungicides.

Fungal plant pathogens cause major crop losses worldwide, with many featuring compartmentalised genomes that include both core and accessory regions, which are believed to drive adaptation. The highly host‐specific fungus Colletotrichum lupini greatly impacts lupin (Lupinus spp.) cultivation. This pathogen is part of clade 1 of the C. acutatum species complex and comprises four genetically uniform, presumably clonal, lineages (I–IV). Despite this, variation in virulence and morphology has been observed within these lineages. To investigate the potential sources of genetic variability in this asexual fungus, we compared the genomes of 16 C. lupini strains and 17 related Colletotrichum species. Phylogenomics confirmed the presence of four distinct lineages, but further examination based on genome size, gene content, transposable elements (TEs), and deletions revealed that lineage II could be split into two groups, II‐A and II‐B. TE content varied between lineages and correlated strongly with genome size variation, supporting a role for TEs in genome expansion in this species. Pangenome analysis revealed a highly variable accessory genome, including a minichromosome present in lineages II, III, and IV, but absent in lineage I. Accessory genes and effectors appeared to cluster in proximity to TEs. Presence/absence variation of putative effectors was lineage‐specific, suggesting that these genes play a crucial role in determining host range. Notably, no effectors were found on the TE‐rich minichromosome. Our findings shed light on the potential mechanisms generating genetic diversity in this asexual fungal pathogen that could aid future disease management. Comparative genomics of the lupin pathogen Colletotrichum lupini reveals low SNP diversity but highlights a dynamic accessory genome, including a variable accessory chromosome and diverse transposable element landscape.

Colletotrichum interacts with numerous plant species overtly as symptomatic pathogens and cryptically as asymptomatic endophytes. It is not known whether these contrasting ecological modes are optional strategies expressed by individual Colletotrichum species or whether a species' ecology is explicitly pathogenic or endophytic. We explored this question by inferring relationships among 77 C. gloeosporioides s.l. strains isolated from asymptomatic leaves and from anthracnose lesions on leaves and fruits of Theobroma cacao (cacao) and other plants from Panamá. ITS and 5′-tef1 were used to assess diversity and to delineate operational taxonomic units for multilocus phylogenetic analysis. The ITS and 5′-tef1 screens concordantly resolved four strongly supported lineages, clades A-D: Clade A includes the ex type of C. gloeosporioides, clade B includes the ex type ITS sequence of C. boninense, and clades C and D are unidentified. The ITS yielded limited resolution and support within all clades, in particular the C. gloeosporioides clade (A), the focal lineage dealt with in this study. In contrast the 5′-tef1 screen differentiated nine distinctive haplotype subgroups within the C. gloeosporioides clade that were concordant with phylogenetic terminals resolved in a five-locus nuclear phylogeny. Among these were two phylogenetic species associated with symptomatic infections specific to either cacao or mango and five phylogenetic species isolated principally as asymptomatic infections from cacao and other plant hosts. We formally describe two new species, C. tropicale and C. ignotum, that are frequent asymptomatic associates of cacao and other Neotropical plant species, and epitypify C. theobromicola, which is associated with foliar and fruit anthracnose lesions of cacao. Asymptomatic Colletotrichum strains isolated from cacao plants grown in China included six distinct C. gloeosporioides clade taxa, only one of which is known to occur in the Neotropics.

Colonization by foliar endophytic fungi can affect the expression of host plant defenses and other ecologically important traits. However, whether endophyte colonization affects the uptake or redistribution of resources within and among host plant tissues remains unstudied. We inoculated leaves of Theobroma cacao with four common colonizers that range in their effect from protective to pathogenic (Colletotrichum tropicale, Pestalotiopsis sp., Colletotrichum theobromicola, or Phytophthora palmivora). We pulsed the soil with nitrogen-15 (15N) and then traced 15N uptake and its subsequent distribution to whole plants and individual leaves. At a whole-plant level, C. tropicale-inoculated plants showed significantly greater 15N uptake than endophyte-free plants did in the same pot. Among leaves within plants, younger leaves were particularly enriched in 15N, but endophyte inoculation at the individual leaf level did not alter 15N distribution within plants. However, leaves co-inoculated with pathogenic Phytophthora and protective C. tropicale experienced significantly elevated 15N content as pathogen damage increased, compared with leaves inoculated only with the pathogen. Further, endophyte–pathogen co-infection also increased total plant biomass. Our results indicate that colonization by foliar endophytes significantly affects N uptake and distribution among and within host plants in ways that appear to be context dependent on other microbiome components.

Three endophytic strains, Phomopsis sp., Fusarium proliferatum , and Tinctoporellus epimiltinus , isolated from various plants in the rainforest of the Philippines, were investigated regarding their ability to repress growth of the pathogenic fungus Colletotrichum musae on banana fruits causing anthracnose disease. An in vitro plate-to-plate assay and an in vivo sealed box assay were conducted, using commercial versus natural potato dextrose medium (PDA). All tested endophytes were able to significantly reduce C . musae growth compared to the control. However, the type of medium had no significant effect on lesion size of C . musae on banana. An interaction effect between fungal strain and medium could be shown. On the commercial medium, no differences between the biocontrol ability of the fungi and control treatments could be found, while there were significant differences between the fungal strains on natural medium. Lesions on banana incubated with Phomopsis sp. on natural medium were significantly but only slightly larger than those on banana incubated with F . proliferatum . Volatiles released by these two strains and one pathogenic strain of F . graminearum were collected using polydimethylsiloxane tubes and analyzed via gas chromatography mass spectrometry (GC-MS). Twelve volatile metabolites were detected. Benzaldehyde was the most prominent volatile emitted from the commercial and plain medium. 2-Undecanone, 2-nonanone, and phenylethyl-alcohol were detected in individual samples in both media. 1-Decanol and acoradiene were exclusive to the commercial medium, with acoradiene also being unique to F . proliferatum . Five volatileorganic compounds (VOCs)were emitted from all tested fungal species: 2-heptanone, 2-nonanone, 2-undecanone, 2-tridecanone, and phenylethyl-alcohol. Beta-acorenol was detected in F . proliferatum grown on both media. To reveal whether the medium (commercial PDA versus potato extract) affected the metabolism of the fungi, metabolic footprints were assessed via high performance liquid chromatography with quadrupole time of flight mass spectrometry MS (HPLC-QTOF-MS). A total of 388 metabolic signals were recorded. The intensities of 80–90% of these signals differed significantly between the two types of media. Metabolic footprints varied in response to different potato dextrose medium preparations. The two promising fungal strains may be used to reduce postharvest decay and losses in fruits.

Colletotrichum infects diverse hosts, including tea plants, and can lead to crop failure. Numerous studies have reported that biological processes are involved in the resistance of tea plants to Colletotrichum spp. However, the molecular and biochemical responses in the host during this interaction are unclear. Cuttings of the tea cultivar Longjing 43 (LJ43) were inoculated with a conidial suspension of Colletotrichum camelliae , and water-sprayed cuttings were used as controls. In total, 10,592 differentially expressed genes (DEGs) were identified from the transcriptomic data of the tea plants and were significantly enriched in callose deposition and the biosynthesis of various phytohormones. Subsequently, 3,555 mass spectra peaks were obtained by LC–MS detection in the negative ion mode, and 27, 18 and 81 differentially expressed metabolites (DEMs) were identified in the tea leaves at 12 hpi, 24 hpi and 72 hpi, respectively. The metabolomic analysis also revealed that the levels of the precursors and intermediate products of jasmonic acid (JA) and indole-3-acetate (IAA) biosynthesis were significantly increased during the interaction, especially when the symptoms became apparent. In conclusion, we suggest that callose deposition and various phytohormone signaling systems play important roles in the tea plant- C. camelliae interaction.

The avocado, Persea americana, is a fruit crop of immense importance to Mexican agriculture with an increasing demand worldwide. Avocado lies in the anciently diverged magnoliid clade of angiosperms, which has a controversial phylogenetic position relative to eudicots and monocots. We sequenced the nuclear genomes of the Mexican avocado race, P. americana var. drymifolia, and the most commercially popular hybrid cultivar, Hass, and anchored the latter to chromosomes using a genetic map. Resequencing of Guatemalan and West Indian varieties revealed that ∼39% of the Hass genome represents Guatemalan source regions introgressed into a Mexican race background. Some introgressed blocks are extremely large, consistent with the recent origin of the cultivar. The avocado lineage experienced 2 lineage-specific polyploidy events during its evolutionary history. Although gene-tree/species-tree phylogenomic results are inconclusive, syntenic ortholog distances to other species place avocado as sister to the enormous monocot and eudicot lineages combined. Duplicate genes descending from polyploidy augmented the transcription factor diversity of avocado, while tandem duplicates enhanced the secondary metabolism of the species. Phenylpropanoid biosynthesis, known to be elicited by Colletotrichum (anthracnose) pathogen infection in avocado, is one enriched function among tandems. Furthermore, transcriptome data show that tandem duplicates are significantly up- and down-regulated in response to anthracnose infection, whereas polyploid duplicates are not, supporting the general view that collections of tandem duplicates contribute evolutionarily recent “tuning knobs” in the genome adaptive landscapes of given species.