故事将衔接TV版第三季结局紫悦(Twilight Sparkle)进化为天角兽(Alicorn)加冕成新公主之后的生活，此时水晶帝国的珍贵王冠被偷窃；为了寻回王冠，紫悦公主将接下重责大任，独自前往另一个平行世界；在那里，紫悦将发现平行世界中的穗龙(Spike)变成了一只狗，而自己则变成了有双手也能双腿站立的人类！身分将改为少女高中生，并重新相遇化身为人类版本的小马朋友们……In Equestria, the newly crowned Princess Twilight Sparkle is still trying to adjust to her new status and wings. However, Sunset Shimmer a renegade former student of Princess Celestia, steals her magic crown and escapes to another world. Twilight is charged with recovering the crown and she and her companion, Spike, pursue the thief. Crossing over, Twilight finds that she has been changed into a powerless human in a high school world populated with teenage human counterparts of her friends. To save both worlds, Twilight must rediscover the magic of friendship that transcends everything she imagined possible.
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