Integrated global analysis in spider flowers illuminates features underlying the evolution and maintenance of C4 photosynthesis

Abstract

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.

Acknowledgements

We thank Prof. Yongqing Jiao at Henan Agricultural University and Prof. Shuangcheng Gao at Henan University of Science and Technology for providing the G. gynandra and T. hassleriana seeds used in this study. This work was supported by the Agricultural Science and Technology Innovation Project of the Chinese Academy of Agricultural Sciences (Grant CAAS-ASTIP-2021-OCRI) and the National Natural Science Foundation of China (Grant 32072096). We appreciate Life Science Editors for editing assistance on the manuscript.

Author contributions

W.H., Jun Liu, and W.Z. conceived project. W.H., Jun Liu, and W.Z. designed study. J.Li, X.S.,Jing Liu and Q.Z., conducted experiments. W.Z. and Jun Liu performed data analysis. W.Z. and Jun Liu wrote and revised the manuscript.

Data availability

All sequence data has been deposited in the Genome Sequence Archive (GSA) (https://bigd.big.ac.cn/gsa). Genomic data: G. gynan- dra-PRJCA017363; transcriptomic data: G. gynandra-PRJCA017364; Tarenaya hassleriana-PRJCA017365. The chromosome-scale annotated genome assembly of G. gynandra is available at the Genome Warehouse in the National Genomics Data Center (NGDC) (https://ngdc.cncb.ac.cn) under accession number GWHCBIX00000000.

Conflict of interest

The authors declare no conflict of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

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