Maturational changes in troponin T expression, Ca2+-sensitivity and twitch contraction kinetics in dragonfly flight muscle

Abstract

Maximum lift production and the thermal sensitivity of lift production increase dramatically during adult maturation of Libellula pulchella dragonflies. Here, we report that the mechanistic basis for this transition appears to involve a developmental change in protein expression, which alters the Ca2+-sensitivity of muscle activation and twitch contraction kinetics. The alternatively spliced Ca2+ regulatory protein troponin T (TnT) undergoes an isoform shift during adult maturation. Skinned (demembranated) fibers of mature flight muscle are up to 13 times more sensitive to activation by Ca2+ than skinned fibers from teneral (newly emerged adult) flight muscle, and their Ca2+-sensitivity is more strongly affected by temperature. Intact muscle from mature individuals has a shorter time to peak tension and longer time to half-relaxation during twitch contractions, which is consistent with a greater Ca2+-sensitivity of mature muscle. Because it becomes activated more quickly and relaxes more slowly, mature flight muscle is able to generate, with each twitch, more force per unit area than teneral muscle; this difference in force becomes greater at high temperatures. There do nut appear to be any age-related differences in actomyosin crossbridge properties, since teneral and mature flight muscles do not differ in shortening velocity, tetanic tension or instantaneous power output during isotonic contraction. Thus, variation in TnT expression appears to affect the temperature-dependent Ca2+-sensitivity of muscle activation, which in turn affects the kinetics and force production of the twitch contractions used by dragonflies during flight. This cascade of effects suggests that maturational changes in the expression of TnT isoforms may be a key determinant of overall muscle and organismal performance.