Abstract

The conidia of a hemibiotrophic fungus, Colletotrichum gloeosporioides, can conventionally form a germ tube (GT) and develop into a fungal colony. Under certain conditions, they tend to get connected through a conidial anastomosis tube (CAT) to share the nutrients. CAT fusion is believed to be responsible for the generation of genetic variations in few asexual fungi, which appears problematic for effective fungal disease management. The physiological and molecular requirements underlying the GT formation versus CAT fusion remained underexplored. In the present study, we have deciphered the physiological prerequisites for GT formation versus CAT fusion in C. gloeosporioides. GT formation occurred at a high frequency in the presence of nutrients, while CAT fusion was found to be higher in the absence of nutrients. Younger conidia were found to form GT efficiently, while older conidia preferentially formed CAT. Whole transcriptome analysis of GT and CAT revealed highly differential gene expression profiles, wherein 11,050 and 9786 genes were differentially expressed during GT formation and CAT fusion, respectively. A total of 1567 effector candidates were identified; out of them, 102 and 100 were uniquely expressed during GT formation and CAT fusion, respectively. Genes coding for cell wall degrading enzymes, germination, hyphal growth, host-fungus interaction, and virulence were highly upregulated during GT formation. Meanwhile, genes involved in stress response, cell wall remodeling, membrane transport, cytoskeleton, cell cycle, and cell rescue were highly upregulated during CAT fusion. To conclude, the GT formation and CAT fusion were found to be mutually exclusive processes, requiring differential physiological conditions and sets of DEGs in C. gloeosporioides. This study will help in understanding the basic CAT biology in emerging fungal model species of the genus Colletotrichum.

Highlights

  • The asexual spore or conidium is essential in the life cycle of many fungi because it is the key for dispersal and serves as a safehouse for the fungi in unfavorable environmental conditions

  • The different stages of the germ tube (GT) formation were determined in C. gloeosporioides, which could be divided into three stages, namely, conidial swelling and adhesion at 3 h post-incubation (Figure 2A,B), GT initiation including polarized growth at 6 hpi (Figure 2B,C), GT elongation with hyphal conidia become primed for conidial anastomosis tube (CAT) fusion as a result of CAT induction (Figure 1A)

  • We propose a model to explain the mutual exclusiveness of GT formation and CAT

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Summary

Introduction

The asexual spore or conidium is essential in the life cycle of many fungi because it is the key for dispersal and serves as a safehouse for the fungi in unfavorable environmental conditions. The conidia germinate to form hyphae and a fully grown fungal colony. The first morphological change in conidial germination is isotropic growth, called the swelling of conidium. The stage is polarized growth that results in forming a germ tube (GT) that extends and successively branches to establish the fungal colony [2]. Under certain conditions such as starvation, a conidium will form specialized hypha, called conidial anastomosis tubes (CATs), instead of forming GTs. The CAT fusion between conidia results in an interconnected germling network, allowing genetic exchange and the sharing of nutrients, water, and cell organelles between conidia [3], which has been theorized to improve survival chances in an adverse environment

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