Not only leaves but also other plant organs and structures typically considered as carbon sinks, including stems, roots, flowers, fruits and seeds, may exhibit photosynthetic activity. There is still a lack of a coherent and systematized body of knowledge and consensus on the role(s) of photosynthesis in these “sink” organs. With regard to fruits, their actual photosynthetic activity is influenced by a range of properties, including fruit anatomy, histology, physiology, development and the surrounding microclimate. At early stages of development fruits generally contain high levels of chlorophylls, a high density of functional stomata and thin cuticles. While some plant species retain functional chloroplasts in their fruits upon subsequent development or ripening, most species undergo a disintegration of the fruit chloroplast grana and reduction in stomata functionality, thus limiting gas exchange. In addition, the increase in fruit volume hinders light penetration and access to CO₂, also reducing photosynthetic activity. This review aimed to compile information on aspects related to fruit photosynthesis, from fruit characteristics to ecological drivers, and to address the following challenging biological questions: why does a fruit show photosynthetic activity and what could be its functions? Overall, there is a body of evidence to support the hypothesis that photosynthesis in fruits is key to locally providing: ATP and NADPH, which are both fundamental for several demanding biosynthetic pathways (e.g., synthesis of fatty acids); O₂, to prevent hypoxia in its inner tissues including seeds; and carbon skeletons, which can fuel the biosynthesis of primary and secondary metabolites important for the growth of fruits and for spreading, survival and germination of their seed (e.g., sugars, flavonoids, tannins, lipids). At the same time, both primary and secondary metabolites present in fruits and seeds are key to human life, for instance as sources for nutrition, bioactives, oils and other economically important compounds or components. Understanding the functions of photosynthesis in fruits is pivotal to crop management, providing a rationale for manipulating microenvironmental conditions and the expression of key photosynthetic genes, which may help growers or breeders to optimize development, composition, yield or other economically important fruit quality aspects.

Climate changes may cause severe impacts both on grapevine and berry development. Foliar application of kaolin has been suggested as a mitigation strategy to cope with stress caused by excessive heat/radiation absorbed by leaves and grape berry clusters. However, its effect on the light micro-environment inside the canopy and clusters, as well as on the acclimation status and physiological responses of the grape berries, is unclear. The main objective of this work was to evaluate the effect of foliar kaolin application on the photosynthetic activity of the exocarp and seeds, which are the main photosynthetically active berry tissues. For this purpose, berries from high light (HL) and low light (LL) microclimates in the canopy, from kaolin-treated and non-treated, irrigated and non-irrigated plants, were collected at three developmental stages. Photochemical and non-photochemical efficiencies of both tissues were obtained by a pulse amplitude modulated chlorophyll fluorescence imaging analysis. The maximum quantum efficiency (F_v/F_m) data for green HL-grown berries suggest that kaolin application can protect the berry exocarp from light stress. At the mature stage, exocarps of LL grapes from irrigated plants treated with kaolin presented higher F_v/F_m and relative electron transport rates (rETR₂₀₀) than those without kaolin. However, for the seeds, a negative interaction between kaolin and irrigation were observed especially in HL grapes. These results highlight the impact of foliar kaolin application on the photosynthetic performance of grape berries growing under different light microclimates and irrigation regimes, throughout the season. This provides insights for a more case-oriented application of this mitigation strategy on grapevines.

The effects of climate change are becoming a real concern for the viticulture sector, with impacts on both grapevine physiology and the quality of the fresh berries and wine. Short-term mitigation strategies, like foliar kaolin application and smart irrigation regimes, have been implemented to overcome these problems. We previously showed that these strategies also influence the photosynthetic activity of the berries themselves, specifically in the exocarp and seed. In the present work, we assessed the modulating effects of both canopy-light microclimate, kaolin and irrigation treatments on the metabolic profiles of the exocarp and seed, as well as the potential role of berry photosynthesis herein. Berries from the white variety Alvarinho were collected at two contrasting light microclimate positions within the vine canopy (HL—high light and LL—low light) from both irrigated and kaolin-treated plants, and their respective controls, at three fruit developmental stages (green, véraison and mature). Untargeted liquid chromatography mass spectrometry (LCMS) profiling of semi-polar extracts followed by multivariate statistical analysis indicate that both the light microclimate and irrigation influenced the level of a series of phenolic compounds, depending on the ripening stage of the berries. Moreover, untargeted gas chromatography mass spectrometry (GCMS) profiling of polar extracts show that amino acid and sugar levels were influenced mainly by the interaction of irrigation and kaolin treatments. The results reveal that both photosynthetically active berry tissues had a distinct metabolic profile in response to the local light microclimate, which suggests a specific role of photosynthesis in these tissues. A higher light intensity within the canopy mainly increased the supply of carbon precursors to the phenylpropanoid/flavonoid pathway, resulting in increased levels of phenolic compounds in the exocarp, while in seeds, light mostly influenced compounds related to carbon storage and seed development. In addition, our work provides new insights into the influence of abiotic stress mitigation strategies on the composition of exocarps and seeds, which are both important tissues for the quality of grape-derived products.

Viticulture practices that change the light distribution in the grapevine canopy can interfere with several physiological mechanisms, such as grape berry photosynthesis and other metabolic pathways, and consequently impact the berry biochemical composition, which is key to the final wine quality. We previously showed that the photosynthetic activity of exocarp and seed tissues from a white cultivar (Alvarinho) was in fact responsive to the light microclimate in the canopy (low and high light, LL and HL, respectively), and that these different light microclimates also led to distinct metabolite profiles, suggesting a berry tissue-specific interlink between photosynthesis and metabolism. In the present work, we analyzed the transcript levels of key genes in exocarps and seed integuments of berries from the same cultivar collected from HL and LL microclimates at three developmental stages, using real-time qPCR. In exocarp, the expression levels of genes involved in carbohydrate metabolism (VvSuSy1), phenylpropanoid (VvPAL1), stilbenoid (VvSTS1), and flavan-3-ol synthesis (VvDFR, VvLAR2, and VvANR) were highest at the green stage. In seeds, the expression of several genes associated with both phenylpropanoid (VvCHS1 and VvCHS3) and flavan-3-ol synthesis (VvDFR and VvLAR2) showed a peak at the véraison stage, whereas that of RuBisCO was maintained up to the mature stage. Overall, the HL microclimate, compared to that of LL, resulted in a higher expression of genes encoding elements associated with both photosynthesis (VvChlSyn and VvRuBisCO), carbohydrate metabolism (VvSPS1), and photoprotection (carotenoid pathways genes) in both tissues. HL also induced the expression of the VvFLS1 gene, which was translated into a higher activity of the FLS enzyme producing flavonol-type flavonoids, whereas the expression of several other flavonoid pathway genes (e.g., VvCHS3, VvSTS1, VvDFR, and VvLDOX) was reduced, suggesting a specific role of flavonols in photoprotection of berries growing in the HL microclimate. This work suggests a possible link at the transcriptional level between berry photosynthesis and pathways of primary and secondary metabolism, and provides relevant information for improving the management of the light microenvironment at canopy level of the grapes.

Lipids and oils determine the quality and industrial value of grape seeds. Studies with legume seeds demonstrated the influence of light on lipid metabolism and its association with seed photosynthesis. Grape berry seeds are photosynthetically active till mature stage, but mostly during the green stage and veraison. The objective of this work was to compare the lipid profiles of seeds from white grape berries (cv. Alvarinho) growing at two contrasting light microclimates in the canopy (low and high light, LL and HL respectively), previously reported to have distinct photosynthetic competences. Berries were collected at three developmental stages (green, veraison and mature) and from both microclimates, and the seeds were analyzed for their lipid profiles in an untargeted manner using liquid chromatography coupled to high resolution mass spectrometry (LCMS). The seed lipid profiles differed greatly among berry developmental stages, and to a lesser extend between microclimates. The LL microclimate coincided with a higher relative levels of fatty acids specifically at mature stage, while the HL microclimate led to an up-regulation of ceramides at green stage and of triacylglycerols and glycerophospholipids at mature stage. The seed transcript levels of four key genes (VvACCase1, VvΔ9FAD, VvFAD6 and VvLOXO) involved in fatty acid metabolism were analyzed using real-time qPCR. The lipoxygenase gene (VvLOXO) was down- and up-regulated by HL, as compared to LL, in seeds at green and veraison stages, respectively. These results suggest that seed photosynthesis may play distinct roles during seed growth and development, possibly by fueling different lipid pathways: at green stage mainly towards the accumulation of membrane-bound lipid species that are essential for cell growth and maintenance of the photosynthetic machinery itself; and at veraison and mature stages mainly towards storage lipids that contribute to the final quality of the grape seeds.