Comparative transcriptomics and eQTL approach identified SlWD40 as a novel tomato fruit ripening regulator

Authors: ZHU, FENG - Max Planck Institute For Biogeochemistry; JADHAV, SAGAR - Max Planck Institute For Biogeochemistry; TOGHE, TAGAYUKI - Max Planck Institute For Biogeochemistry; SALEM, MOHAMED - Menoufia University; LI, JEMIN - Boyce Thompson Institute; Giovannoni, James; CHENG, YUNJIANG - Huazhong Agricultural University; ALSEEKH, SALEH - Max Planck Institute For Biogeochemistry; FERNIE, ALISDAIR - Max Planck Institute For Biogeochemistry

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/28/2022
Publication Date: 5/4/2022
Citation: Zhu, F., Jadhav, S., Toghe, T., Salem, M., Li, J., Giovannoni, J.J., Cheng, Y., Alseekh, S., Fernie, A. 2022. Comparative transcriptomics and eQTL approach identified SlWD40 as a novel tomato fruit ripening regulator. Plant Physiology. https://doi.org/10.1093/plphys/kiac200.
DOI: https://doi.org/10.1093/plphys/kiac200

Interpretive Summary: Given that seed dispersal is of major ecological and evolutionary importance for all plants and the fact that fleshy fruit plays a vital role in this process, fruit ripening assumes a central importance in the plant life-cycle. It is well documented that hundreds of genes display altered expression during this process, and that metabolism also undergoes dramatic shifts to bring about important aspects of fruit quality including color, flavor and texture. Here we identified a gene called SlWD40 and demonstrated its central role in ripening. Repression of the gene resulted in altered ripening suggesting that natural variation of SlWD40 could be selected for in breeding to optimize ripening quality of tomato fruit.

Technical Abstract: Although multiple vital genes with strong effects on the tomato (Solanum lycopersicum) ripening process have been identified via the positional cloning of ripening mutants and cloning of ripening-related transcription factors, recent studies suggest that it is unlikely that we have fully characterized the gene regulatory networks underpinning this process. Here, combining comparative transcriptomics and eQTLs, we identified 16 candidate genes involved in tomato fruit ripening and validated them through virus-induced gene silencing (VIGS) analysis. To further confirm the accuracy of the approach, one potential ripening regulator, SlWD40 (WD-40 repeats), was chosen for in-depth analysis. Co-expression network analysis indicated that master regulators such as RIN (ripening inhibitor) and NOR (nonripening) as well as vital transcription factors including FUL1 (FRUITFUL1), SlNAC4 (NAM, ATAF1,2 and CUC2 4), and AP2a (Activating enhancer binding Protein 2 alpha) strongly co-expressed with SlWD40. Furthermore, SlWD40 overexpression and RNAi lines exhibited substantially accelerated and delayed ripening phenotypes compared to the WT, respectively. Moreover, transcriptome analysis of these transgenics revealed that expression patterns of ethylene biosynthesis genes, phytoene synthase (PSY), pectate lyase (PL), and branched chain amino transferase 2 (BCAT2), in SlWD40-RNAi lines were similar to those of rin and nor fruits, which further demonstrated that SlWD40 may act as an important ripening regulator in conjunction with RIN and NOR. These results are discussed in the context of current models of ripening and in terms of the use of comparative genomics and transcriptomics as an effective route for isolating causal genes underlying differences in genotypes.