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Article|20 Jun 2023|OPEN
Integrated global analysis in spider flowers illuminates features underlying the evolution and maintenance of C4 photosynthesis 
Wei Zhao1 ,† , Jun Li1 ,† , Xingchao Sun1 , Qiwei Zheng1 , Jing Liu1,2 and Wei Hua1,2 , , Jun Liu,1 ,
1Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture and Rural Affairs, Oil Crops Research Institute of the Chinese Academy of Agricultural Sciences, Wuhan 430062, China
2Hubei Hongshan Laboratory, Wuhan 430070, China
*Corresponding author. E-mail:,
Both authors contributed equally to the study.

Horticulture Research 10,
Article number: uhad129 (2023)
Views: 103

Received: 12 Feb 2023
Accepted: 11 Jun 2023
Published online: 20 Jun 2023


The carbon concentrating mechanism—C4 photosynthesis—represents a classic example of convergent evolution, but how this important trait originated and evolved remains largely enigmatic. The spider flower Gynandropsis gynandra is a valuable leafy vegetable crop and medicinal plant that has also been recognized as a C4 model species. Here we present a high-quality chromosome-scale annotated genome assembly of G. gynandra through a combination of Oxford Nanopore Technology (ONT), HiFi and Hi-C technology. The 17 super-scaffolds cover 98.66% of the estimated genome (997.61 Mb), with a contig N50 of 11.43 Mb and a scaffold N50 of 51.02 Mb. Repetitive elements occupy up to 71.91% of its genome, and over half are long terminal repeat retrotransposons (LTR-RTs) derived from recent bursts, contributing to genome size expansion. Strikingly, LTR-RT explosion also played a critical role in C4 evolution by altering expression features of photosynthesis-associated genes via preferential insertion in promoters. Integrated multiomics analyses of G. gynandra and the ornamental horticulture C3 relative Tarenaya hassleriana reveal that species-specific whole-genome duplication, gene family expansion, recent LTR–RT amplification, and more recent tandem duplication events have all facilitated the evolution of C4 photosynthesis, revealing uniqueness of C4 evolution in the Cleome genus. Moreover, high leaf vein density and heat stress resilience are associated with shifted gene expression patterns. The mode of C3-to-C4 transition found here yields new insights into evolutionary convergence of a complex plant trait. The availability of this reference-grade genomic resource makes G. gynandra an ideal model system facilitating efforts toward C4-aimed crop engineering.