The giant genomes of lily provide insights into the evolution of Liliales

Liliales are monocots with enormous evolutionary, ecological, and economic significance worldwide. We report the reference genome sequences for both lily and flame lily of Liliales. We reveal evolutionary, molecular insights, and valuable genomic information of the unique lily plants.
The giant genomes of lily provide insights into the evolution of Liliales
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The Liliales order is one of the most important orders of angiosperms comprising a diverse range of monocot plants, many of which have substantial economic, ecological, and ornamental importance, no genome sequences of any species within the Liliales order have been published so far. 

L. sargentiae E.H.Wilson, L. regale E.H.Wilson, and L. davidii E. H. Wilson were introduced to American and European gardens by famous plant hunter E. H. Wilson and played a crucial role in preserving American and European lilies during the 18th century. Therefore, we chose L. sargentiae performs genome sequencing. 

Gloriosa superba, also known as flame lily and a member of the Colchicaceae family, holds significance not only as a popular ornamental crop renowned for its striking flame-like flowers but also as the primary natural source of colchicine. Colchicine is abundantly present in G. superba rhizomes and is effectively used in treating gout, arthritis, and inflammation as well as inducing polyploidy in plants.

Both lilies and flame lilies exhibit unique biological features, the modified stem-originated rootstocks, with lilies having bulbs and flame lilies possessing rhizomes. In this study, the genome of L. sargentiae and G. superba was obtained. Their pictures are as follows.

 

Lily (L.sargentiae)

 flame lily (G. superba) 

Our discoveries will contribute significantly to the assembly and understanding of giant plant genomes, shed light on hybridization patterns in cultivated lilies, uncover the genetic mechanisms behind the formation of rhizomes and bulbs, and provide insights into specialized biological pathways such as the colchicine metabolic pathway in lilies and/or flame lilies. These breakthroughs represent major advancements in the field of genomics and evolution of Liliales, extending even to a broader spectrum of flowering plants.

The five highlights of our resource paper below:

1. In this study, a total of approximately 27 Tb of sequencing data for the genome of L. sargentiae and G. superba was obtained. We present the reference genome assemblies for both L. sargentiae (47.09 Gb) and G. superba (5.15 Gb). Notably, we discovered that L. sargentiae possesses the largest sequenced plant genome published to date, surpassing even the lungfish genomes (40.05 Gb and 36.53 Gb, the largest sequenced eukaryotic genomes). We found continuous proliferation of long terminal repeat retroelements (LTR-RTs) during recent evolution in both L. sargentiae and G. superba genomes, and the more pronounced activity of LTR-RTs in the L. sargentiae genome has shaped the giant lily genome.

2. Although the genomes of eightmonocot orders have been sequenced, the order Liliales, which includes economically significant crops such as lilies and tulips, has yet to be sequenced. Therefore, completing the genome sequencing of Liliales is of great importance for enhancing the genomic landscape of monocot plants. By incorporating two genome of lilies into our study, we have successfully bridged this critical knowledge gap. This achievement contributes significantly to a deeper understanding and further research on the evolution, functions, and genetic traits of monocot plants. Furthermore, our analysis has revealed lineage-specific whole genome duplication (WGD) events in both lilies and flame lilies, shedding light on the evolutionary trajectories within Liliaceae and Colchicaceae.

3. Our most comprehensive phylogenomic relationships of51 wild Lilium plants and 34 different lily cultivars has provided valuable insights into the relationships between major wild and cultivated lily species. We have revealed several instances of independent origins of lily hybrids, shedding light on their complex genetic origins. Notably, our findings highlight that numerous wild lilies have not been involved in hybridization events with the main cultivated lily species. This discovery underscores the presence of a previously untapped genetic reservoir, offering immense potential for future breeding endeavors. The utilization of these untapped genetic resources holds great value and promise for advancements in lily breeding programs.

4. While genomes of other rhizome and/or bulb plants, such as Salvia miltiorrhiza, ginger, and garlic, have been previously documented, there is still a lack of comprehensive understanding regarding the evolution of rhizomes and bulbs. Additionally, the underlying genetic mechanisms responsible for their formation, as well as the related regulatory genes involved, have not been clearly elucidated at the functional genomics level. To address this gap in knowledge, we conducted a systematic exploration of bulb and rhizome formationusing the genomes of these two lily species. This investigation also involved the identification of relevant functional genes, including XTHs (xyloglucan endotransglucosylases/hydrolases), which significantly contribute to advancing the field of functional genomics research on bulbs and rhizomes. These findings have implications for gene mining and utilization of rhizomes and bulbs, further enhancing our understanding and utilization of these plant structures.

5. The colchicine synthesis pathway was successfully elucidated using transcriptome data from G. superba. This pathway had not been previously resolved at the genome level due to the unavailability of the G. superba genome. By utilizing the G. superba genome, along with RNA-seq and metabolic data, we were able to identify gene clusters responsible for colchicine biosynthesis, which are unique to the flame lily species. Notably, the absence of specific colchicine-related clusters in L. sargentiae suggests that this plant species lacks the ability to synthesize colchicine. These findings indicate that colchicine biosynthesis likely originated independently within the Colchicaceae family.

 Specifically, our discoveries will contribute significantly to the assembly and understanding of giant plant genomes, shed light on hybridization patterns in cultivated lilies, uncover the genetic mechanisms behind the formation of rhizomes and bulbs, and provide insights into specialized biological pathways such as the colchicine metabolic pathway in lilies and/or flame lilies. These breakthroughs represent major advancements in the field of genomics and evolution of Liliales, extending even to a broader spectrum of flowering plants.

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Agriculture
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