Abstract
Diverse fungi live all or part of their life cycle inside plants as asymptomatic endophytes. While endophytic fungi are increasingly recognized as significant components of plant fitness, it is unclear how they interact with plant cells; why they occur throughout the fungal kingdom; and why they are associated with most fungal lifestyles. Here we evaluate the diversity of endophytic fungi that are able to form novel protoplasts called mycosomes. We found that mycosomes cultured from plants and phylogenetically diverse endophytic fungi have common morphological characteristics, express similar developmental patterns, and can revert back to the free-living walled state. Observed with electron microscopy, mycosome ontogeny within Aureobasidium pullulans may involve two organelles: double membrane-bounded promycosome organelles (PMOs) that form mycosomes, and multivesicular bodies that may form plastid-infecting vesicles. Cultured mycosomes also contain a double membrane-bounded organelle, which may be homologous to the A. pullulans PMO. The mycosome PMO is often expressed as a vacuole-like organelle, which alternatively may contain a lipoid body or a starch grain. Mycosome reversion to walled cells occurs within the PMO, and by budding from lipid or starch-containing mycosomes. Mycosomes discovered in chicken egg yolk provided a plant-independent source for analysis: they formed typical protoplast stages, contained fungal ITS sequences and reverted to walled cells, suggesting mycosome symbiosis with animals as well as plants. Our results suggest that diverse endophytic fungi express a novel protoplast phase that can explain their hidden existence, lifestyle switching, and diversity within the plant kingdom. Importantly, our findings outline “what, where, when and how”, opening the way for cell and organelle-specific tests using in situ DNA hybridization and fluorescent labels. We discuss developmental, ecological and evolutionary contexts that provide a robust framework for continued tests of the mycosome phase hypothesis.
Highlights
Ancient fungi evolved an unprecedented ability to live all or part of their life cycle inside plants, joining these two lineages in an extraordinary example of coevolutionary radiation
Mycosome ontogeny within A. pullulans: electron microscopy
Fungal promycosome organelles (PMOs) are mistaken for lipid bodies, perhaps one factor contributing to their crypsis
Summary
Ancient fungi evolved an unprecedented ability to live all or part of their life cycle inside plants, joining these two lineages in an extraordinary example of coevolutionary radiation. While some endophytes are observed within and between plant cells, the largest group (Class 3; [3]) form imperceptible infections that are apparently localized, i.e., their internal hyphal phase is limited or seemingly non-existent These cryptic endophytes are typically discovered by DNA sequencing or by fungal isolation from small samples of cultured plant tissue [4,5,6,7,8,9,10,11,12]. The mystery is compounded because cryptic endophytes lack a clear physical presence, yet emerge as walled cells from cultured plant tissues The assumption that these fungi express an internal walled state is generally untested and has encouraged the default hypothesis that many endophytes persist as one or a few latent cells until they emerge and sporulate during host-tissue senescence. Somehow these ‘quiescent’ endophytes are biochemically coevolved [15,16] and sufficiently active to benefit their hosts in multiple ways [3,8,17,18,19,20,21]
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