Cucumber STACHYOSE SYNTHASE is regulated by its cis-antisense RNA asCsSTS to balance source–sink carbon partitioning

Abstract

Photosynthate partitioning between source and sink is a key determinant of crop yield. In contrast to sucrose-transporting plants, cucumber (Cucumis sativus) plants mainly transport stachyose and stachyose synthase (CsSTS) synthesizes stachyose in the vasculature for loading. Therefore, CsSTS is considered a key regulator of carbon partitioning. We found that CsSTS expression and CsSTS enzyme activity were upregulated in the vasculature and downregulated in mesophyll tissues at fruiting. In situ hybridization and tissue enrichment experiments revealed that a cis-natural antisense noncoding transcript of CsSTS, named asCsSTS, is mainly expressed in mesophyll tissues. In vitro overexpression (OE), RNA interference (RNAi) and dual luciferase reporter experiments indicated that CsSTSs are negatively regulated by asCsSTS. Fluorescence in situ hybridization revealed that asCsSTS transcript localized in leaf cytoplasm, indicating that the regulation of CsSTS by asCsSTS is a posttranscriptional process. Further investigation revealed that this regulation occurred by reducing CsSTS transcript stability through a DICER-like protein-mediated pathway. Chemically induced OE and RNAi of asCsSTS led to promotion or inhibition, respectively, of assimilate export from leaves and altered fruit growth rates. Our results suggest that the regulation of CsSTSs between the mesophyll and vasculature reduces sugar storage in mesophyll tissue and promotes assimilate export from the leaf when the plant carries fruit.

Long Exposure to Salt Stress Leads to Stronger Damage in Chloroplast Ultrastructure and its Functionality than the Stomatal Function in<em> Jatropha curcas</em>

“…As previously demonstrated, larger starch granules promote the destruction of thylakoid lamellae and then a secondary reduction in the photosynthetic rate [79]. Furthermore, favourable conditions must be present for phloem loading, which appear to be regulated by genes of the type CsSTS (Cucumis sativus stachyose synthase) [80], StSUT2 (Spondias tuberosa sucrose transporter 2) [81], and SWEET4 superfamily of genes [82]. However, when the metabolism is reduced, the expression of genes involved in phloem loading may also be compromised, and as a consequence, more starch granules are formed into the chloroplast [83][84][85].…”

The Sink-Source Relationship in Cucumber (Cucumis sativus L.) Is Modulated by DNA Methylation

“…It has been reported that in the sucrose metabolism pathway, gene expression and enzyme activity associated with sucrose catabolism (SUS, invertase, etc.) decrease under low source-sink ratio conditions [ 16 ]. In our work, two SUS genes ( CsaV3_4G000970 and CsaV3_5G020420 ) were downregulated in FNLs, suggesting that a feedback regulatory mechanism in the sink-source relationship may lead to less sucrose being synthesized in leaves.…”

“…The leaves and fast-growing fruits belong to the “source” and “sink” organs in cucumber. Cucumber is a typical raffinose family oligosaccharide (RFO)-transporting plant, determining that the sink-source regulation of cucumber differs from sucrose-transporting model plants, such as Arabidopsis ( Arabidopsis thaliana ), rice ( Oryza sativa ) and tomato ( Solanum lycopersicum ) [ 14 , 15 , 16 , 17 ]. The proportion of RFO in cucumber leaf assimilates is up to 80%, which is unique to RFO-transporting plants [ 18 ].…”

“…For example, Liu et al [ 20 ] reported that the expression of alkaline α-galactosidase 2 ( CsAGA2 ) in fruit is essential for cucumber sink strength and showed feedback regulation on source leaves. Dai et al [ 16 ] demonstrated that the expression of CsSTS was significantly elevated in leaves with fast-growing fruit, promoting assimilate loading into the vascular tissue.…”

The Inferior Grain Filling Initiation Promotes the Source Strength of Rice Leaves

“…However, the heavy carbohydrate accumulation of leaves can repress photosynthesis and regulate sugar distribution in plants (Goldschmidt and Huber 1992 ; Ainsworth and Bush 2011 ). Several studies have shown that sink strength plays a crucial role for controlling plants growth and the rate of photosynthetic activity in source leaves (Sonnewald and Fernie 2018 ; Xu et al 2021 ; Cabon et al 2022 ; Dai et al 2023 ). The activities associated with high sink growth need to consider not only the efficiency of photo-assimilate production and sucrose transport, but also the sink's capacity to utilize carbohydrates (Chen et al 2019 ; Jiang et al 2021 ).…”