Wang Yinggang, Li Xinhui, Qiu Huixia, Chen Ruting, Xiong Aisheng, Xu Zhisheng, Miao Wu, Chen Rugang, Wang Peizhi, Hou Xilin, Yu Huiyang, Yang Bozhi, Yang Sha, Suo Huan, Zou Xuexiao, Liu Zhoubin, Ou Lijun
Key Laboratory for Vegetable Biology of Hunan Province, Engineering Research Center for Horticultural Crop Germplasm Creation and New Variety Breeding, Ministry of Education, College of Horticulture, Hunan Agricultural University, Changsha 410125, China.
College of Horticulture, Nanjing Agricultural University, 1 Weigang, Nanjing 210095, China.
Plant Physiol. 2025 Feb 7;197(2). doi: 10.1093/plphys/kiaf013.
Carotenoids play indispensable roles in the ripening process of fleshy fruits. Capsanthin is a widely distributed and utilized natural red carotenoid. However, the regulatory genes involved in capsanthin biosynthesis remain insufficient. Here, we identified the MADS-box transcription factor RIPENING INHIBITOR (MADS-RIN) in pepper (Capsicum annuum), which regulates ripening in climacteric tomato (Solanum lycopersicum) fruits, using weighted gene co-expression network analysis. We found MADS-RIN can directly bind to the promoters of carotenoid biosynthetic genes phytoene synthase 1 (PSY1) and capsanthin/capsorubin synthase (CCS) and the promoter of DIVARICATA1 to activate their expression, thereby regulating carotenoid biosynthesis directly or indirectly. The physical interaction between MADS-RIN and DIVARICATA1 enhances the transactivation effect on PSY1 and CCS. The self-transactivation of MADS-RIN demonstrates its capability to expedite the above process under specific conditions. Interestingly, chromatin immunoprecipitation sequencing assays revealed consistency and divergence of potential targets of MADS-RIN in climacteric tomato and nonclimacteric pepper fruits, suggesting potential conservation and variation of MADS-RIN in regulating ripening and carotenoid metabolism. The present study illustrates the regulatory mechanism of the MADS-RIN-DIVARICATA1 module in capsanthin biosynthesis in pepper, providing targets for breeding high-quality peppers. These findings enrich our understanding of the regulatory network of carotenoid biosynthesis and offer insights into the complex mechanisms of MADS-RIN in climacteric/nonclimacteric fruit ripening and carotenoid biosynthesis.
类胡萝卜素在肉质果实的成熟过程中发挥着不可或缺的作用。辣椒红素是一种广泛分布且被利用的天然红色类胡萝卜素。然而，参与辣椒红素生物合成的调控基因仍然不足。在此，我们利用加权基因共表达网络分析，在辣椒（Capsicum annuum）中鉴定出了成熟抑制因子（MADS-RIN），该因子在跃变型番茄（Solanum lycopersicum）果实中调控成熟过程。我们发现MADS-RIN可以直接结合类胡萝卜素生物合成基因八氢番茄红素合成酶1（PSY1）和辣椒红素/辣椒玉红素合成酶（CCS）的启动子以及DIVARICATA1的启动子，以激活它们的表达，从而直接或间接调控类胡萝卜素的生物合成。MADS-RIN与DIVARICATA1之间的物理相互作用增强了对PSY1和CCS的反式激活作用。MADS-RIN的自我反式激活证明了其在特定条件下加速上述过程的能力。有趣的是，染色质免疫沉淀测序分析揭示了MADS-RIN在跃变型番茄和非跃变型辣椒果实中的潜在靶标的一致性和差异，表明MADS-RIN在调控成熟和类胡萝卜素代谢方面可能存在保守性和变异性。本研究阐明了辣椒中MADS-RIN-DIVARICATA1模块在辣椒红素生物合成中的调控机制，为培育高品质辣椒提供了靶点。这些发现丰富了我们对类胡萝卜素生物合成调控网络的理解，并为MADS-RIN在跃变型/非跃变型果实成熟和类胡萝卜素生物合成中的复杂机制提供了见解。
