Transcriptional networks orchestrating red and pink testa color in peanut

Authors: AHMAD, NAVEED - Shandong Academy Of Agricultural Sciences; ZHANG, KUN - Shandong Academy Of Agricultural Sciences; MA, JING - Shandong Academy Of Agricultural Sciences; YUAN, MEI - Shandong Academy Of Agricultural Sciences; HAO, SHUZHEN - Shandong Academy Of Agricultural Sciences; WANG, MINGQING - Shandong Peanut Research Institute; DENG, LI - Shandong University; REN, LI - Shandong University; GANGURDE, SUNIL - University Of Georgia; PAN, JIAOWEN - Shandong Academy Of Agricultural Sciences; MA, CHANGLE - Shandong Agricultural University; LI, CHANGSHENG - Shandong Academy Of Agricultural Sciences; Guo, Baozhu; WANG, XINGJUN - Shandong Academy Of Agricultural Sciences; LI, AIQIN - Shandong Academy Of Agricultural Sciences; ZHAO, CHUANZHI - Shandong Academy Of Agricultural Sciences

Submitted to: BMC Plant Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/3/2023
Publication Date: 1/23/2023
Citation: Ahmad, N., Zhang, K., Ma, J., Yuan, M., Hao, S., Wang, M., Deng, L., Ren, L., Gangurde, S.S., Pan, J., Ma, C., Li, C., Guo, B., Wang, X., Li, A., Zhao, C. 2023. Transcriptional networks orchestrating red and pink testa color in peanut. BMC Plant Biology. 23:44. https://doi.org/10.1186/s12870-023-04041-0.
DOI: https://doi.org/10.1186/s12870-023-04041-0

Interpretive Summary: Peanut is one of the important cash crops widely known for its high-quality edible oil and rich nutritional value. It is particularly interesting to human health for a variety of nutritional ingredients like isoflavones, vitamins (vitamin B1, B3, B9, and E), anthocyanin, and procyanidins that are synthesized in peanut testa. Different peanut testa color is associated with a range of anthocyanin contents and controlled by different genes. Therefore, this study investigated the molecular mechanism in association with gene expression in peanut lines with red and pink testa, which were selected from a mapping population derived from a Red testa parent and a pink testa parent. The data suggested the identification of candidate functional genes and potential strategies for manipulation of anthocyanin biosynthesis pathway to improve peanut cultivars with different pigmentation in peanut testa and the associated levels of anthocyanin resulting in potential added nutritional values.

Technical Abstract: Testa color is an important trait of peanut (Arachis hypogaea L.) which is closely related with the nutritional and commercial value. Pink and red are main color of peanut testa. However, the genetic mechanism of testa color regulation in peanut is not fully understood. To elucidate a clear picture of peanut testa regulatory model, samples of pink cultivar Y9102, red cultivar ZH12, and two RNA pools (bulk red and bulk pink) from F2 lines of Y9102 x ZH12 were compared through a bulk RNA-seq approach. A total of 2,992 differential expressed genes (DEGs) were identified. There were 317 and 1,334 genes up-regulated and 225 and 1,116 genes down-regulated in the bulk red-vs-bulk pink RNA pools and Y9102-vs-ZH12, respectively. KEGG analysis indicates that these genes were divided into significantly enriched metabolic pathways including phenylpropanoid, flavonoid/anthocyanin, isoflavonoid and lignin biosynthetic pathways. Noticeably, the increased expression of the anthocyanin upstream regulatory genes such as PAL, CHS, and CHI in both testa peanuts suggests that their regulation may occur much earlier than the emergence of testa pigmentation. However, the differential expression of down-stream regulatory genes including F3H, DFR, and ANS revealed that deepening of testa color not only depends on their gene expression bias, but also linked with FLS inhibition. In addition, the downregulation of HCT, IFS, HID, 7-IOMT, and I2'H genes provided an alternative mechanism for promoting anthocyanin accumulation via perturbation of lignin and isoflavone pathways, which may be used as a novel strategy to improve peanuts with various testa color. Furthermore, the co-expression of MYB, bHLH, and WRKY transcription factors also provides a fascinating transcriptional activation complex, where MYB-bHLH could utilize WRKY as a co-option during the regulation of peanut testa color by augmenting anthocyanin biosynthesis. These findings reveal candidate functional genes and potential strategies for the manipulation of anthocyanin biosynthesis to improve peanut varieties with desirable testa color.