Integrated responses to altered carbohydrate availability during seed development in Arabidopsis thaliana

Abstract

Seed development depends on an adequate carbohydrate supply from the maternal plant that must be balanced with demand, to ensure viable seed production. Losses in seed yield during environmental stress, often due to reduced carbohydrate availability to reproductive organs, highlights the importance of this balance. The aim of this project was to investigate the effect of heat stress (HS) on seed development. This was achieved by subjecting Arabidopsis plants to different regimes of day- or night-time, or continuous HS, and determining the effects on embryo and endosperm development. HS resulted in acute, stage-specific inhibition of embryo development. During continuous HS, embryos undergoing morphogenesis were delayed and had morphological abnormalities, leading to arrest and seed abortion. Embryos beyond morphogenesis were less sensitive and grew to maturity. HS also affected nuclear divisions in the endosperm syncytium before seeds reached their final size. Similar delays were seen during day- or night-time only HS; however, seed viability was not affected. Expression of HS markers showed immediate perception of HS. Observed effects of HS on reproductive growth were linked, at least partially, to altered carbohydrate status in the plant. Leaf starch turnover showed time-of-day-specific effects. Developing siliques and inflorescences contained more sucrose than the controls. Together with upregulation of genes encoding sucrose transporters involved in phloem loading, these findings suggest preferential allocation of sugars to the reproductive organs during HS. However, how sucrose reaches early embryos undergoing morphogenesis is largely unknown. Gene expression analysis revealed putative involvement of AtSWEET4, AtSWEET8, AtSWEET10 and AtCWINV4 – encoding sucrose-efflux and cell-wall invertase proteins – in post-phloem flow of sucrose in seeds. Embryo development was delayed in plants carrying one or more sweet and cwinv null alleles, indicating important roles for these proteins during seed development, providing promising targets to improve yields under HS. Overall, delayed embryo development in sweet;cwinv mutant plants and acute inhibition of early embryogenesis during HS, is linked to impaired carbohydrate utilisation rather than provision from the maternal plant. Together with developmental stage-specific sensitivities, these findings have significant implications for seed yield stability under HS.