Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, College of Horticulture, China Agricultural University, Beijing 100193, China.
Key Laboratory of Biology and Genetic Improvement of Horticultural Crops of the Ministry of Agriculture, Sino-Dutch Joint Laboratory of Horticultural Genomics, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China.
Plant Physiol. 2022 Jun 27;189(3):1501-1518. doi: 10.1093/plphys/kiac152.
Sugars are necessary for plant growth and fruit development. Cucumber (Cucumis sativus L.) transports sugars, mainly raffinose family oligosaccharides (RFOs), in the vascular bundle. As the dominant sugars in cucumber fruit, glucose and fructose are derived from sucrose, which is the product of RFO hydrolysis by α-galactosidase (α-Gal). Here, we characterized the cucumber alkaline α-galactosidase 2 (CsAGA2) gene and found that CsAGA2 has undergone human selection during cucumber domestication. Further experiments showed that the expression of CsAGA2 increases gradually during fruit development, especially in fruit vasculature. In CsAGA2-RNA interference (RNAi) lines, fruit growth was delayed because of lower hexose production in the peduncle and fruit main vascular bundle (MVB). In contrast, CsAGA2-overexpressing (OE) plants displayed bigger fruits. Functional enrichment analysis of transcriptional data indicated that genes related to sugar metabolism, cell wall metabolism, and hormone signaling were significantly downregulated in the peduncle and fruit MVBs of CsAGA2-RNAi plants. Moreover, downregulation of CsAGA2 also caused negative feedback regulation on source leaves, which was shown by reduced photosynthetic efficiency, fewer plasmodesmata at the surface between mesophyll cell and intermediary cell (IC) or between IC and sieve element, and downregulated gene expression and enzyme activities related to phloem loading, as well as decreased sugar production and exportation from leaves and petioles. The opposite trend was observed in CsAGA2-OE lines. Overall, we conclude that CsAGA2 is essential for cucumber fruit set and development through mediation of sugar communication between sink strength and source activity.
糖是植物生长和果实发育所必需的。黄瓜（Cucumis sativus L.）通过维管束运输糖，主要是棉子糖家族低聚糖（RFOs）。作为黄瓜果实中的主要糖，葡萄糖和果糖来源于蔗糖，蔗糖是α-半乳糖苷酶（α-Gal）水解 RFO 的产物。在这里，我们对黄瓜碱性α-半乳糖苷酶 2（CsAGA2）基因进行了表征，并发现 CsAGA2 在黄瓜驯化过程中经历了人类选择。进一步的实验表明，CsAGA2 的表达在果实发育过程中逐渐增加，特别是在果实维管束中。在 CsAGA2-RNA 干扰（RNAi）系中，由于花梗和果实主维管束（MVB）中六碳糖产量较低，果实生长受到延迟。相比之下，CsAGA2 过表达（OE）植物的果实更大。转录数据的功能富集分析表明，CsAGA2-RNAi 植物花梗和果实 MVB 中与糖代谢、细胞壁代谢和激素信号转导相关的基因显著下调。此外，CsAGA2 的下调也对源叶产生了负反馈调节，表现为光合效率降低，叶肉细胞和中间细胞（IC）或 IC 和筛管之间表面的质膜通道减少，与韧皮部装载相关的基因表达和酶活性下调，以及叶片和叶柄的糖产生和输出减少。在 CsAGA2-OE 系中观察到相反的趋势。总的来说，我们得出结论，CsAGA2 通过介导源活性和汇强度之间的糖通讯，对黄瓜果实结实和发育是必不可少的。
