Carbohydrate metabolism and gene regulation during anther development in an androdioecious tree, Tapiscia sinensis

Abstract

• Background and Aims Tapiscia sinensis (Tapisciaceae) is a functional androdioecious species with both male and hermaphroditic individuals, and fruit ripening overlaps with flowering in the hermaphroditic individuals. Pollen vitality was lower in the hermaphrodites than in the males. Anther development requires nutrients, and carbohydrates are the basic nutrients; abnormal carbohydrate metabolism will result in pollen abortion. The aim of this research was to gain insight into the relationship between carbohydrate metabolism and the weakening of the male function of hermaphroditic flowers in T. sinensis. • Methods Observation of morphology and microscopic and sub-microscopic structures was carried out. Sugar measurements and quantitative real-time PCR analysis were performed for the genes related to sugar metabolism and transport in the development of anthers in both males and hermaphrodites. The expression pattern of Cell wall invertase 2 (CWI2) and Sucrose transporter 2 (ST2) was explored by in situ hybridization. • Key Results At the vacuolate microspore (VM) stage, polysaccharides accumulated in the connective tissue of the hermaphroditic anthers, and the levels of total soluble sugar, sucrose and starch in the hermaphroditic anthers were significantly lower than in the male anthers. Most of the hermaphroditic pollen grains were empty, with degradation of the cytoplasm, absence of an intine layer and defective exines. There was a significant differential expression between male and hermaphroditic flowers of several key genes that are involved in sugar metabolism, transport and intine development. CWI2 and ST2 were expressed in the tapetum and microspores. The expression of CWI2 was significantly lower in hermaphrodites than in the males. • Conclusions Fruit ripening overlaps with flowering, leading to a severe reproductive burden on the hermaphroditic individuals. The hermaphroditic flowers regulating carbohydrate metabolism and transport to affect resources are biased towards the female function to ensure reproduction, causing a deficiency in resources for the development of pollen; thus, the pollen viability is lower. This makes it easier for males to invade the hermaphroditic population and form a functional androdioecious breeding system.