Remodelling of mitochondria during spermiogenesis of Chinese soft-shelled turtle (Pelodiscus sinensis)

Abstract

Mitochondria are vital cellular organelles that have the ability to change their shape under different conditions, such as in response to stress, disease, changes in metabolic rate, energy requirements and apoptosis. In the present study, we observed remodelling of mitochondria during spermiogenesis and its relationship with mitochondria-associated granules (MAG). At the beginning of spermiogenesis, mitochondria are characterised by their round shape. As spermiogenesis progresses, the round-shaped mitochondria change into elongated and then swollen mitochondria, subsequently forming a crescent-like shape and finally developing into onion-like shaped mitochondria. We also noted changes in mitochondrial size, location and patterns of cristae at different stages of spermiogenesis. Significant differences (P<0.0001) were found in the size of the different-shaped mitochondria. In early spermatids transitioning to the granular nucleus stage, the size of the mitochondria decreased, but increased subsequently during spermiogenesis. Changes in size and morphological variations were achieved through marked mitochondrial fusion. We also observed a non-membranous structure (MAG) closely associated with mitochondria that may stimulate or control fusion during mitochondrial remodelling. The end product of this sophisticated remodelling process in turtle spermatozoa is an onion-like mitochondrion. The acquisition of this kind of mitochondrial configuration is one strategy for long-term sperm storage in turtles.

Mitochondrial Features and Expressions of MFN2 and DRP1 during Spermiogenesis in Phascolosoma esculenta

“…The distribution of mitochondria during spermatogenesis in several animals, including (but not limited to) Mollusca [ 23 ], Arthropoda [ 24 ], Pisces [ 25 ], Reptile [ 26 ], and Mammalia [ 27 , 28 ], has been reported. In Octopus tankahkeei , the mitochondria are randomly distributed in the cytoplasm of early spermatids: some are polarized to the tail to form the midpiece, and some migrate to the top of the (eventual) sperm head and are discarded with the cytoplasm in the late stage of spermiogenesis [ 23 ].…”

“…In Pelodiscus sinensis , mitochondria are randomly distributed in early spermatids and are gradually distributed near the membrane during spermatid development. The mitochondria are distributed along the outer dense fibers in the midpiece in the late maturation phase [ 26 ]. In Rattus norvegicus , mitochondria are distributed in the cell periphery in the Golgi phase, cap phase, and early acrosome phases of spermiogenesis and move to the flagellum in the late acrosome and early maturation phases.…”

“…The morphological features of mitochondria during spermatogenesis in several animals, including Arthropoda [ 24 ], Pisces [ 29 ], Reptile [ 26 ], and Mammalia [ 17 ], have also been reported. In D. melanogaster , small mitochondria aggregate and eventually fuse to form two large mitochondria (which constitute a nebenkern in spermatid) during spermatogenesis [ 24 ].…”

“…In sperm, the mitochondria are approximately circular and uniform in size [ 29 ]. In Pelodiscus sinensis , the mitochondria are round in the early spermatid phase, gradually elongate in the middle spermatid phase, fuse in the late spermatid phase, and eventually become onion-shaped in sperm [ 26 ]. In R. norvegicus , orthodox-type mitochondria are usually found in spermatogonia and preleptotene and leptotene spermatocytes, intermediate-type mitochondria are usually found in synaptene spermatocytes, late spermatids, and sperm, and condensed-type mitochondria are usually found in pachytene spermatocytes, secondary spermatocytes, and early spermatids [ 12 , 17 ].…”

Mouse TMCO5 is localized to the manchette microtubules involved in vesicle transfer in the elongating spermatids

“…Secondly, drastic morphological changes occur by developing cytoskeleton systems to create novel structures [4]. Thirdly, in order to acquire the ability of movement, energy-producing mitochondria are densely packed to the midpiece [5], and a flagellum is constructed to the tail. Fourthly, the functions required for fertilization are equipped; acrosome for passing the zona pellucida [6], proteins for cell membrane fusion [7, 8], and protein kinases for activating eggs [9, 10].…”