Spatio-temporal remodeling of extracellular matrix orients epithelial sheet folding

Abstract

Biological systems are inherently noisy; however, they produce highly stereotyped tissue morphology. Drosophila pupal wings show a highly stereotypic folding through uniform expansion and subsequent buckling of wing epithelium within a surrounding cuticle sac. The folding pattern produced by buckling is generally stochastic; it is thus unclear how buckling leads to stereotypic tissue folding of the wings. We found that the extracellular matrix (ECM) protein, Dumpy, guides the position and direction of buckling-induced folds. Dumpy anchors the wing epithelium to the overlying cuticle at specific tissue positions. Tissue-wide alterations of Dumpy deposition and degradation yielded different buckling patterns. In summary, we propose that spatio-temporal ECM remodeling shapes stereotyped tissue folding through dynamic interactions between the epithelium and its external structures.

Histological Observation of Helmet Development in the Treehopper Poppea capricornis (Insecta: Hemiptera: Membracidae)

“…The suprahumeral horns seem to be formed by using the nymphal suprahumeral buds as a mold, while the posterior horns are made without any nymphal mold structure. Recent studies suggest that a combination of epithelial cell sheet contraction and adhesion of this sheet to old cuticle plays an important role in the development of adult structures (Matsuda et al, 2023;Tsuboi et al, 2023). We hypothesized that the posterior horns are also generated by a combination of contraction during miniature formation and adhesion between the nymphal helmet sheath cuticle and dorsal layer of the developing adult helmet.…”

Wings expansion inDrosophila melanogaster

“…The biological and physical mechanisms by which these transformations are coordinated in space and time are a central issue in developmental biology. The wing of the fruit fly Drosophila melanogaster is a paradigmatic example of such continuous organ-scale transformation, combining expansion and buckling of the wing epithelium to shape the pupal wings into a highly folded origami structure [6±9]. However, how the origami unfolds into a functional wing within minutes after emergence remains largely unknown.…”

Post-embryonic tail development through molting of the freshwater shrimpNeocaridina denticulata

“…During the prepupal-pupal period, the individuals are macroscopically immobile while the morphogenetic process occurs. Therefore, in vivo live imaging studies are being performed in Drosophila (10)(11)(12). On the other hand, in hemimetabolous insects, particularly Gryllus, it is becoming possible to describe the developmental process and perform some advanced genetic manipulation (13,14), however live imaging of morphological changes through molting is not yet available.…”