TY - JOUR
T1 - An Alternative Self-Splicing Intron Lifecycle Revealed by Dynamic Intron Turnover in Epichloë Endophyte Mitochondrial Genomes
AU - Chan, Jennie
AU - Truglio, Mauro
AU - Schardl, Christopher L.
AU - Cox, Murray P.
AU - Young, Carolyn A.
AU - Ganley, Austen R.D.
N1 - Publisher Copyright:
© The Author(s) 2025.
PY - 2025/4/1
Y1 - 2025/4/1
N2 - Self-splicing group I and II introns are selfish genetic elements that are widely yet patchily distributed across the tree of life. Their selfish behavior comes from super-Mendelian inheritance behaviors, collectively called “homing”, which allow them to rapidly spread within populations to the specific genomic sites they home into. Observations of self-splicing intron evolutionary dynamics have led to the formulation of an intron “lifecycle” model where, once fixed in a population, the introns lose selection for homing and undergo an extensive period of degradation until their eventual loss. Here, we find that self-splicing introns are common in the mitochondrial genomes of Epichloë species, endophytic fungi that live in symbioses with grasses. However, these introns show substantial intron presence–absence polymorphism, with our analyses suggesting that these result from a combination of vertical intron inheritance coupled with multiple invasion and loss events over the course of Epichloë evolution. Surprisingly, we find little evidence for the extensive intron degradation expected under the existing intron lifecycle model. Instead, these introns in Epichloë appear to be lost soon after fixation, suggesting that Epichloë self-splicing introns have a different lifecycle. However, rapid intron loss alone cannot explain our results, indicating that additional factors, such as the evolution of homing suppressors, also contribute to Epichloë self-splicing intron dynamics. This work shows that self-splicing introns have more diverse evolutionary dynamics than previously appreciated.
AB - Self-splicing group I and II introns are selfish genetic elements that are widely yet patchily distributed across the tree of life. Their selfish behavior comes from super-Mendelian inheritance behaviors, collectively called “homing”, which allow them to rapidly spread within populations to the specific genomic sites they home into. Observations of self-splicing intron evolutionary dynamics have led to the formulation of an intron “lifecycle” model where, once fixed in a population, the introns lose selection for homing and undergo an extensive period of degradation until their eventual loss. Here, we find that self-splicing introns are common in the mitochondrial genomes of Epichloë species, endophytic fungi that live in symbioses with grasses. However, these introns show substantial intron presence–absence polymorphism, with our analyses suggesting that these result from a combination of vertical intron inheritance coupled with multiple invasion and loss events over the course of Epichloë evolution. Surprisingly, we find little evidence for the extensive intron degradation expected under the existing intron lifecycle model. Instead, these introns in Epichloë appear to be lost soon after fixation, suggesting that Epichloë self-splicing introns have a different lifecycle. However, rapid intron loss alone cannot explain our results, indicating that additional factors, such as the evolution of homing suppressors, also contribute to Epichloë self-splicing intron dynamics. This work shows that self-splicing introns have more diverse evolutionary dynamics than previously appreciated.
KW - epichloe
KW - homing endonuclease
KW - intron
KW - mitochondrial genome
KW - self-splicing
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U2 - 10.1093/molbev/msaf076
DO - 10.1093/molbev/msaf076
M3 - Article
C2 - 40172118
AN - SCOPUS:105003280730
SN - 0737-4038
VL - 42
JO - Molecular Biology and Evolution
JF - Molecular Biology and Evolution
IS - 4
M1 - msaf076
ER -