Ultrastructural evolution, physiological traits, and carbon and nitrogen assimilation–related gene expression are compatible with the developmental transitions of parthenogenesis in Pyropia haitanensis (Bangiales, Rhodophyta)

Abstract

Pyropia haitanensis has a typical parthenogenetic behavior under unisexual culture condition. In this study, ultrastructural evolution and physiological traits of photosynthesis and the expression characteristics of key enzyme genes related to carbon and nitrogen assimilation pathways at different developmental stages of parthenogenesis were analyzed. Ultrastructural observations showed that the gametophytic vegetative cells had cell wall, pyrenoids, abundant chloroplasts, and rarely scattered floridean starch grains. However, the appearance of gathered chloroplasts, plastoglobuli, large lipid droplets, pyrenoids encircled by numerous plastoglobuli, and an increased number of floridean starch grains in the cells during parthenogenesis provide neutral lipid and energy resources that are compatible with the developmental transitions. Physiologically, vegetative gametophytes possessed the highest Fv/Fm and Chl. a content and the lowest C/N ratio. However, compared with vegetative cell proliferation stage, the activities of RubisCO (ribulose bisphosphate carboxylase) and external CA (carbonic anhydrase) increased at early stages of parthenogenesis, and Fv/Fm and activities of PEPC (phosphoenolpyruvate carboxylase) and PEPCK (phosphoenolpyruvate carboxykinase) remained higher at later stages of parthenogenesis, suggesting that dynamic photosynthetic carbon fixation occurs in parthenogenesis. Quantitative real-time PCR analysis showed that selective regulation of key enzyme genes related to carbon and nitrogen assimilation pathways maintained stable carbon and nitrogen metabolism during developmental transitions of parthenogenesis. Moreover, during parthenogenesis, photosynthetic carbon fixation pathway potentially changed from C3 pathway at female gametophyte stage to C4 pathway at parthenosporophyte stage, which is similar to that of gametophytes and sporophytes in sexual reproduction. Meanwhile, the ammonia assimilation involved GDH pathway (glutamate dehydrogenase pathway) and GS/GOGAT cycle (glutamine synthetase/glutamate synthase cycle) in female gametophyte stage, while GS/GOGAT cycle was dominant in parthenosporophyte stage, suggesting that GS/GOGAT cycle may play an important role in the carbon and nitrogen balance during the developmental transitions of parthenogenesis. These results provide important information for revealing the adaptation strategy of parthenogenesis in Pyropia.