Aerobic respiration by haemocyanin in the embryo of the migratory locust.

It remains unresolved how insect embryos acquire sufficient oxygen to sustain high rates of respiratory metabolism during embryogenesis in the absence of a fully developed tracheal system. Our previous work showed that the two distinct subunits (Hc1 and Hc2) of haemocyanin (Hc), a copper-containing protein, display embryo-specific high expression that is essential for embryonic development and survival in the migratory locust Locusta migratoria. Here we investigated the role of haemocyanins in oxygen sensing and supply in the embryo of this locust. Putative binding sites for hypoxia-regulated transcription factors were identified in the promoter region of all of the Hc1 and Hc2 genes. Embryonic expression of haemocyanins was highly upregulated by ambient O deprivation, up to 10-fold at 13% O content. The degree of upregulation of haemocyanins increased with increasing levels of hypoxia. Compared with low-altitude locusts, embryonic expression of haemocyanins in high-altitude locusts from Tibetan plateau was constitutively higher and more robust to oxygen deprivation. These findings strongly suggest an active involvement of haemocyanins in oxygen exchange in embryos. We thus propose a mechanistic model for embryo respiration in which haemocyanin plays a key role by complementing the tracheal system for oxygen transport during embryogenesis.