Roles of Intra-fruit Oxygen and Carbon Dioxide in Controlling Pepper (Capsicum annuum L.) Seed Development and Storage Reserve Deposition

Abstract

<jats:p>Seeds developing within a locular space inside hollow fruit experience chronic exposure to a unique gaseous environment. Using two pepper cultivars, `Triton' (sweet) and `PI 140367' (hot), we investigated how the development of seeds is affected by the gases surrounding them. The atmospheric composition of the seed environment was characterized during development by analysis of samples withdrawn from the fruit locule with a gas-tight syringe. As seed weight plateaued during development, the seed environment reached its lowest O<jats:sub>2</jats:sub> concentration (19%) and highest CO<jats:sub>2</jats:sub> concentration (3%). We experimentally manipulated the seed environment by passing different humidified gas mixtures through the fruit locule at a rate of 60 to 90 mL·min<jats:sup>-1</jats:sup>. A synthetic atmosphere containing 3% CO<jats:sub>2</jats:sub>, 21% O<jats:sub>2</jats:sub>, and 76% N<jats:sub>2</jats:sub> was used to represent a standard seed environment. Seeds developing inside locules supplied with this mixture had enhanced average seed weight, characterized by lower variation than in the no-flow controls due to fewer low-weight seeds. The importance of O<jats:sub>2</jats:sub> in the seed microenvironment was demonstrated by reduction in seed weight when the synthetic atmosphere contained only 15% O<jats:sub>2</jats:sub> and by complete arrest of embryo development when O<jats:sub>2</jats:sub> was omitted from the seed atmosphere. Removal of CO<jats:sub>2</jats:sub> from the synthetic atmosphere had no effect on seed weight, however, the CO<jats:sub>2</jats:sub>-free treatment accelerated fruit ripening by 4 days in the hot pepper. In the sweet peppers, fruit wall starch and sucrose were reduced by the CO<jats:sub>2</jats:sub>-free treatment. The results demonstrate that accretionary seed growth is being limited in pepper by O<jats:sub>2</jats:sub> availability and suggest that variation in seed quality is attributable to localized limitations in O<jats:sub>2</jats:sub> supply.</jats:p>

High-resolution spatiotemporal transcriptome mapping of tomato fruit development and ripening

“…We propose that despite its location, the pericarp inner epidermis of tomato fruit is most likely photosynthetically active, and may play a role in the photoassimilation of CO 2 from the fruit locular cavity, as has been suggested to be the case in the dry, dehiscent pea fruit/pod 50 . The high expression of photosynthetic genes in the inner epidermis may also contribute to maintaining sufficient O 2 in the locular cavity for successful seed development, since such a role for O 2 has been suggested in pepper ( Capsicum annuum ) fruit 51 . The cell-type-dependent gene expression profiling therefore highlights clear spatial variation in central carbon metabolism across the pericarp and provides a platform for investigating mechanisms by which sugars traffic between, and are distributed among, the constituent cell types.…”

Simulating in ovulo osmotic potentials and O2 tensions normalize growth and pigmentation of immature cotton embryos

“…species with simple fleshy fruits (berries, drupes, pomes, and pepos), follicles, nuts, and other species similar to cotton in producing thick capsules. It is likely that ovary wall photosynthesis recycles much of the CO 2 released into locules of such plants by respiring cells of the ovule(s) and other fruit tissues, and the resulting production of O 2 by the ovary wall is likely important to normal seed development (Blasiak et al 2006).…”

Brassica rapa L. seed development in hypergravity

“…Removing seeds from this microenvironment disrupts this co-regulation, so procedures that would directly measure respiration or photosynthesis rates by the immature seeds are not practical because they disturb this equilibrium. Non-invasive experiments on the seed microenvironment performed with a range of model species have led us to conclude that seed development in green pepper (Blasiak and Musgrave, 2002; Blasiak et al , 2006), Arabidopsis (Kuang et al , 1998) and Brassica (Porterfield et al , 1999; Musgrave et al , 2008) is oxygen limited. When plants were grown in a range of sub-ambient oxygen concentrations, the growth of their developing embryos was proportional to the amount of oxygen in the surrounding atmosphere (Kuang et al , 1998).…”

“…When plants were grown in a range of sub-ambient oxygen concentrations, the growth of their developing embryos was proportional to the amount of oxygen in the surrounding atmosphere (Kuang et al , 1998). Similarly, pepper fruits that developed with synthetic internal gases passing through their locular spaces would mature their seeds normally if the gas composition mimicked what occurs normally inside the fruit (Blasiak et al , 2006). Raising the O 2 concentration in the flow-through mixture by even a few per cent resulted in larger seeds with more advanced storage reserve deposition (Blasiak et al , 2006).…”

“…Similarly, pepper fruits that developed with synthetic internal gases passing through their locular spaces would mature their seeds normally if the gas composition mimicked what occurs normally inside the fruit (Blasiak et al , 2006). Raising the O 2 concentration in the flow-through mixture by even a few per cent resulted in larger seeds with more advanced storage reserve deposition (Blasiak et al , 2006). Comparison of storage reserve deposition in cotyledons of Brassica seeds developing in vitro (shown to be a more oxygen-limited environment than in vivo ) revealed that the loss of starch and formation of lipids are retarded by oxygen restriction to the developing seeds (Musgrave et al , 2008).…”