The telomere-to-telomere genome of Pucai (蒲菜) (Typha angustifolia L.): a distinctive semiaquatic vegetable with lignin and chlorophyll as quality characteristics

Ya-Peng Li , Li-Yao Su , Ting Huang , Hui Liu , Shan-Shan Tan , Yuan-Jie Deng , Ya-Hui Wang , Ai-Sheng Xiong

Horticulture Research ›› 2025, Vol. 12 ›› Issue (7) : 79

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Horticulture Research ›› 2025, Vol. 12 ›› Issue (7) :79 DOI: 10.1093/hr/uhaf079
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The telomere-to-telomere genome of Pucai (蒲菜) (Typha angustifolia L.): a distinctive semiaquatic vegetable with lignin and chlorophyll as quality characteristics
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Abstract

Pucai (蒲菜) (Typha angustifolia L.), within the Typha spp., is a distinctive semiaquatic vegetable. Lignin and chlorophyll are two crucial traits and quality indicators for Pucai. In this study, we assembled a 207.00-Mb high-quality gapless genome of Pucai, telomere-to-telomere (T2T) level with a contig N50 length of 13.73 Mb. The most abundant type of repetitive sequence, comprising 16.98% of the genome, is the long terminal repeat retrotransposons (LTR-RT). A total of 30 telomeres and 15 centromeric regions were predicted. Gene families related to lignin, chlorophyll biosynthesis, and disease resistance were greatly expanded, which played important roles in the adaptation of Pucai to wetlands. The slow evolution of Pucai was indicated by the σ whole-genome duplication (WGD)-associated Ks peaks from different Poales and the low activity of recent LTR-RT in Pucai. Meanwhile, we found a unique WGD event in Typhaceae. A statistical analysis and annotation of genomic variations were conducted in interspecies and intraspecies of Typha. Based on the T2T genome, we constructed lignin and chlorophyll metabolic pathways of Pucai. Subsequently, the candidate structural genes and transcription factors that regulate lignin and chlorophyll biosynthesis were identified. The T2T genomic resources will provide molecular information for lignin and chlorophyll accumulation and help to understand genome evolution in Pucai.

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Ya-Peng Li, Li-Yao Su, Ting Huang, Hui Liu, Shan-Shan Tan, Yuan-Jie Deng, Ya-Hui Wang, Ai-Sheng Xiong. The telomere-to-telomere genome of Pucai (蒲菜) (Typha angustifolia L.): a distinctive semiaquatic vegetable with lignin and chlorophyll as quality characteristics. Horticulture Research, 2025, 12(7): 79 DOI:10.1093/hr/uhaf079

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Acknowledgements

This article was supported by the Priority Academic Program Development of Jiangsu Higher Education Institutions Project (PAPD), Coordinated Extension of Major Agricultural Technologies Program of Jiangsu (2022-ZYXT-01-3). The study was supported by the Bioinformatics Center of Nanjing Agricultural University. Thanks to Associate Professor Guang-Long Wang from Huaiyin Institute of Technology and Associate Professor Ling-Yun Chen from China Pharmaceutical University for the assistance.

Author contributions

A.S.X. initiated and designed the research. Y.P.L. and L.Y.S. performed the experiments. Y.P.L., L.Y.S., T.H., H.L., S.S.T., Y.J.D., and Y.H.W. analyzed the data. A.S.X. contributed reagents/materials/analysis tools. Y.P.L. wrote the paper. A.S.X. and Y.P.L. revised the paper. All authors read and approved of the final manuscript.

Data availability

The assembled Pucai genome can be downloaded from the NCBI (https://www.ncbi.nlm.nih.gov/) database with the BioProject accession number PRJNA1221093. The transcriptome sequencing data generated in this study have been deposited in the NCBI Sequence Read Archive (SRA) database under accession number PRJNA1221065. The date is available in the figures of the article and its supplementary materials.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1]

Zhou B, Tu T, Kong F. et al. Revised phylogeny and historical biogeography of the cosmopolitan aquatic plant genus Typha (Typhaceae). Sci Rep. 2018; 8:8813

[2]

Claudia C, Heather K, Jeffrey RR. et al. Intercontinental dispersal of Typha angustifolia and T. latifolia between Europe and North America has implications for Typha invasions. Biol Invasions. 15: 1377-90

[3]

Smith SG. Experimental and natural hybrids in North American Typha (Typhaceae). Am Midl Nat. 1967; 78:257-87

[4]

Smith SG. Typha: its taxonomy and the ecological significance of hybrids. Arch Hydrobiol. 1987; 27:129-38

[5]

Liao Y, Zhao S, Zhang W. et al. Chromosome-level genome and high nitrogen stress response of the widespread and ecologi-cally important wetland plant Typha angustifolia. Front Plant Sci. 2023; 14:1138498

[6]

Feng G, Ai X, Yi H. et al. Genomic and transcriptomic analyses of Citrus sinensis varieties provide insights into Valencia orange fruit mastication trait formation. Hortic Res. 2021; 8:218

[7]

Boerjan W, Ralph J, Baucher M. Lignin biosynthesis. Annu Rev Plant Biol. 2003; 54:519-46

[8]

Vanholme R, De MB, Ralph J. et al. Lignin biosynthesis and its integration into metabolism. Curr Opin Biotech. 2019; 56:230-9

[9]

Liu Q, Luo L, Zheng L. Lignins: biosynthesis and biological func-tions in plants. Int J Mol Sci. 2018; 19:335

[10]

Bonawitz ND, Chapple C. The genetics of lignin biosynthesis: connecting genotype to phenotype. Annu Rev Genet. 2010; 44: 337-63

[11]

Vogt T. Phenylpropanoid biosynthesis. Mol Plant. 2010; 3:2-20

[12]

Miao YC, Liu CJ. ATP-binding cassette-like transporters are involved in the transport of lignin precursors across plasma and vacuolar membranes. Proc Natl Acad Sci USA. 2010; 107: 22728-33

[13]

Hoffmann N, Benske A, Betz H. et al. Laccases and peroxidases co-localize in lignified secondary cell walls throughout stem development. Plant Physiol. 2020; 184:806-22

[14]

Wang R, Xue Y, Fan J. et al. A systems genetics approach reveals PbrNSC as a regulator of lignin and cellulose biosynthesis in stone cells of pear fruit. Genome Biol. 2021; 22:313

[15]

Zeng JK, Li X, Xu Q. et al. EjAP2-1, an AP2/ERF gene, is a novel regulator of fruit lignification induced by chilling injury, via interaction with EjMYB transcription factors. Plant Biotechnol J. 2015; 13:1325-34

[16]

Zeng J, Li X, Zhang J. et al. Regulation of loquat fruit low tem-perature response and lignification involves interaction of heat shock factors and genes associated with lignin biosynthesis. Plant Cell Environ. 2016; 39:1780-9

[17]

Jiang C, Lyu K, Zeng S. et al. A combined metabolome and transcriptome reveals the lignin metabolic pathway during the developmental stages of peel coloration in the ‘Xinyu’ pear. Int J Mol Sci. 2024; 25:7481

[18]

YanC, HuZ, NieZ. et al. CcBLH6, a bell-like homeodomain-containing transcription factor, regulates the fruit lignification pattern. Planta. 2021; 253:90

[19]

Willows RD. Biosynthesis of chlorophylls from protoporphyrin IX. Nat Prod Rep. 2003; 20:327-41

[20]

Eckhardt U, Grimm B, Hörtensteiner S. Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol Biol. 2004; 56:1-14

[21]

Vavilin DV, Vermaas WFJ. Regulation of the tetrapyrrole biosyn-thetic pathway leading to heme and chlorophyll in plants and cyanobacteria. Physiol Plant. 2002; 115:9-24

[22]

Tanaka A, Tanaka R. Chlorophyll metabolism. Curr Opin Plant Biol. 2006; 9:248-55

[23]

Takamiya KI, Tsuchiya T, Ohta H. Degradation pathway(s) of chlorophyll: what has gene cloning revealed? Trends Plant Sci. 2000; 5:426-31

[24]

Nagata N, Tanaka R, Satoh S. et al. Identification of a vinyl reductase gene for chlorophyll synthesis in Arabidopsis thaliana and implications for the evolution of prochlorococcus species. Plant Cell. 2005; 17:233-40

[25]

Rzeznicka K, Warlker CJ, Westergren T. et al. Xantha-l encodes a membrane subunit of the aerobic Mg-protoporphyrin IX monomethyl ester cyclase involved in chlorophyll biosynthesis. Proc Natl Acad Sci USA. 2005; 102:5886-91

[26]

Suzuki T, Kunieda T, Murai F. et al. Mg-dechelation activ-ity in radish cotyledons with artificial and native substrates, Mg-chlorophyllin a and chlorophyllide a. Plant Physiol Biochem. 2005; 43:459-64

[27]

Frangedakis E, Yelina NE, Billakurthi K. et al. MYB-related transcription factors control chloroplast biogenesis. Cell. 2024; 187:4859-4876.e22

[28]

Kim N, Jeong J, Kim J. et al. Shade represses photosynthetic genes by disrupting the DNA binding of GOLDEN2-LIKE1. Plant Physiol. 2023; 191:2334-52

[29]

Luo F, Cai JH, Kong XM. et al. Transcriptome profiling reveals the roles of pigment mechanisms in postharvest broccoli yellowing. Hortic Res. 2019; 6:74

[30]

SongB, NingWD, WeiD. et al. Plant genome resequencing and population genomics: current status and future prospects. Mol Plant. 2023; 16:1252-68

[31]

Widanagama SD, Freeland JR, Xu X. et al. Genome assembly, annotation, and comparative analysis of the cattail Typha lati-folia. G3 (Bethesda). 2022;12:jkab401

[32]

Chen J, Wang Z, Tan K. et al. A complete telomere-to-telomere assembly of the maize genome. Nat Genet. 2023; 55:1221-31

[33]

Huang J, Zhang Y, Li Y. et al. Haplotype-resolved gapless genome and chromosome segment substitution lines facilitate gene identification in wild rice. Nat Commun. 2024; 15:4573

[34]

Han X, Zhang Y, Zhang Q. et al. Two haplotype-resolved, gap-free genome assemblies for Actinidia latifolia and Actinidia chinensis shed light on the regulatory mechanisms of vitamin C and sucrose metabolism in kiwifruit. Mol Plant. 2023; 16:452-70

[35]

Li Q, Qiao X, Li L. et al. Haplotype-resolved T2T genome assem-blies and pangenome graph of pear reveal diverse patterns of allele-specific expression and the genomic basis of fruit quality traits. Plant Commun. 2024; 5:101000

[36]

Li K, Chen R, Abudoukayoumu A. et al. Haplotype-resolved T2T reference genomes for wild and domesticated accessions shed new insights into the domestication of jujube. Hortic Res. 2024;11:uhae071

[37]

Liu W, Xu S, Ou C. et al. T2T genomes of carrot and Alternaria dauci and their utility for understanding host-pathogen inter-actions during carrot leaf blight disease. Plant J. 2024; 120: 1643-61

[38]

Wang YH, Liu PZ, Liu H. et al. Telomere-to-telomere carrot (Dau-cus carota) genome assembly reveals carotenoid characteristics. Hortic Res. 2023;10:uhad103

[39]

Garg V, Bohra A, Mascher M. et al. Unlocking plant genetics with telomere-to-telomere genome assemblies. Nat Genet. 2024; 56: 1788-99

[40]

Shakirov EV, Chen JJ-L, Shippen DE. Plant telomere biology: the green solution to the end-replication problem. Plant Cell. 2022; 34: 2492-504

[41]

Ou S, Chen J, Jiang N. Assessing genome assembly quality using the LTR assembly index (LAI). Nucleic Acids Res. 2018; 46:e126

[42]

Masand M, Sharma S, Kumari S. et al. High-quality haplotype-resolved chromosome assembly provides evolutionary insights and targeted steviol glycosides (SGs) biosynthesis in Stevia rebau-diana Bertoni. Plant Biotechnol J. 2024; 22:3262-77

[43]

Guo X, Wang F, Fang D. et al. The genome of Acorus deciphers insights into early monocot evolution. Nat Commun. 2023; 14: 3662

[44]

Shi T, Huneau C, Zhang Y. et al. The slow-evolving Acorus tatari-nowii genome sheds light on ancestral monocot evolution. Nat Plants. 2022; 8:764-77

[45]

Givnish TJ, Barfuss MH, Van Ee B. et al. Adaptive radiation, corre-lated and contingent evolution, and net species diversification in Bromeliaceae. Mol Phylogenet Evol. 2014; 71:55-78

[46]

Magallón S, Gómez-Acevedo S, Sánchez-Reyes LL. et al. Ameta-calibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytol. 2015; 207:437-53

[47]

Tang H, Bowers JE, Wang X. et al. Angiosperm genome compar-isons reveal early polyploidy in the monocot lineage. Proc Natl Acad Sci USA. 2010; 107:472-7

[48]

Jiao Y, Li J, Tang H. et al. Integrated syntenic and phylogenomic analyses reveal an ancient genome duplication in monocots. Plant Cell. 2014; 26:2792-802

[49]

Soltis PS, Soltis DE. Ancient WGD events as drivers of key inno-vations in angiosperms. Curr Opin Plant Biol. 2016; 30:159-65

[50]

Wang W, Haberer G, Gundlach H. et al. The Spirodela polyrhiza genome reveals insights into its neotenous reduction fast growth and aquatic lifestyle. Nat Commun. 2014; 5:3311

[51]

Ming R, VanBuren R, Wai CM. et al. The pineapple genome and the evolution of CAM photosynthesis. Nat Genet. 2015; 47: 1435-42

[52]

Paterson AH, Bowers JE, Bruggmann R. et al. The Sorghum bicolor genome and the diversification of grasses. Nature. 2009; 457: 551-6

[53]

Wang X, Wang J, Jin D. et al. Genome alignment spanning major Poaceae lineages reveals heterogeneous evolutionary rates and alters inferred dates for key evolutionary events. Mol Plant. 2015; 8:885-98

[54]

Panchy N, Lehti-Shiu M, Shiu SH. Evolution of gene duplication in plants. Plant Physiol. 2016; 171:2294-316

[55]

Deng Y, Liu S, Zhang Y. et al. A telomere-to-telomere gap-free reference genome of watermelon and its mutation library provide important resources for gene discovery and breeding. Mol Plant. 2022; 15:1268-84

[56]

Fu A, Zheng Y, Guo J. et al. Telomere-to-telomere genome assem-bly of bitter melon (Momordica charantia L. var. abbreviata Ser.) reveals fruit development, composition and ripening genetic characteristics. Hortic Res. 2023;10:uhac228

[57]

Nie S, Zhao SW, Shi TL. et al. Gapless genome assembly of azalea and multi-omics investigation into divergence between two species with distinct flower color. Hortic Res. 2023;10: uhac241

[58]

Altemose N, Logsdon GA, Bzikadze AV. et al. Complete genomic and epigenetic maps of human centromeres. Science. 2022;376: eabl4178

[59]

Naish M, Alonge M, Wlodzimierz P. et al. The genetic and epigenetic landscape of the Arabidopsis centromeres. Science. 2021;374:eabi7489

[60]

Shang L, He W, Wang T. et al. A complete assembly of the rice Nipponbare reference genome. Mol Plant. 2023; 16:1232-6

[61]

Ma PF, Liu YL, Jin GH. et al. The Pharus latifolius genome bridges the gap of early grass evolution. Plant Cell. 2021; 33:846-64

[62]

Bansal S, Shane CL, Sue N. et al. Typha (cattail) invasion in North American wetlands: biology, regional problems, impacts, ecosystem services, and management. Wetlands. 2019; 39:645-84

[63]

Zhang T, Peng W, Xiao H. et al. Population genomics highlights structural variations in local adaptation to saline coastal envi-ronments in woolly grape. J Integr Plant Biol. 2024; 66:1408-26

[64]

Rai PK. Heavy metal pollution in aquatic ecosystems and its phytoremediation using wetland plants: an ecosustainable approach. Int J Phytoremediation. 2008; 10:131-58

[65]

Wu Z, Wang N, Hisano H. et al. Simultaneous regulation of F5H in COMT-RNAi transgenic switchgrass alters effects of COMT suppression on syringyl lignin biosynthesis. Plant Biotechnol J. 2019; 17:836-45

[66]

Dong NQ, Lin HX. Contribution of phenylpropanoid metabolism to plant development and plant-environment interactions. J Integr Plant Biol. 2021; 63:180-209

[67]

Gallego-Giraldo L, Liu C, Pose-Albacete S. et al. ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE 1 (ADPG1) releases latent defense signals in stems with reduced lignin content. Proc Natl Acad Sci USA. 2020; 117:3281-90

[68]

Wang X, Zhuo C, Xiao X. et al. Substrate specificity of LACCASE8 facilitates polymerization of caffeyl alcohol for C-lignin biosyn-thesis in the seed coat of Cleome hassleriana. Plant Cell. 2020; 32: 3825-45

[69]

Fitter DW, Martin DJ, Copley MJ. et al. GLK gene pairs regu-late chloroplast development in diverse plant species. Plant J. 2002; 31:713-27

[70]

Yasumura Y, Moylan EC, Langdale JA. A conserved transcrip-tion factor mediates nuclear control of organelle biogenesis in anciently diverged land plants. Plant Cell. 2005; 17:1894-907

[71]

Powell AL, Nguyen CV, Hill T. et al. Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloro-plast development. Science. 2012; 336:1711-5

[72]

Shimizu T, Kacprzak SM, Mochizuki N. et al. The retrograde signaling protein GUN1 regulates tetrapyrrole biosynthesis. Proc Natl Acad Sci USA. 2019; 116:24900-6

[73]

Martín G, Leivar P, Ludevid D. et al. Phytochrome and ret-rograde signalling pathways converge to antagonistically reg-ulate a light-induced transcriptional network. Nat Commun. 2016; 7:11431

[74]

Kolmogorov M, Yuan J, Lin Y. et al. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol. 2019; 37:540-6

[75]

Cheng H, Concepcion GT, Feng X. et al. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat Methods. 2021; 18:170-5

[76]

Zhang X, Zhang S, Zhao Q. et al. Assembly of allele-aware, chromosomal-scale autopolyploid genomes based on Hi-C data. Nat Plants. 2019; 5:833-45

[77]

Poplin R, Chang PC, Alexander D. et al. A universal SNP and small-indel variant caller using deep neural networks. Nat Biotechnol. 2018; 36:983-7

[78]

Jain C, Rhie A, Zhang H. et al. Weighted minimizer sam-pling improves long read mapping. Bioinformatics. 2020;36: i111-8

[79]

Manni M, Berkeley MR, Seppey M. et al. BUSCO update: novel and streamlined workflows along with broader and deeper phyloge-netic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol Biol Evol. 2021; 38:4647-54

[80]

Song JM, Xie WZ, Wang S. et al. Two gap-free reference genomes and a global view of the centromere architecture in rice. Mol Plant. 2021; 14:1757-67

[81]

Holt C, Yandell M. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics. 2011; 12:491

[82]

Sun P, Jiao B, Yang Y. et al. WGDI: a user-friendly toolkit for evo-lutionary analyses of whole-genome duplications and ancestral karyotypes. Mol Plant. 2022; 15:1841-51

[83]

Sun M, Yao C, Shu Q. et al. Telomere-to-telomere pear (Pyrus pyrifolia) reference genome reveals segmental and whole genome duplication driving genome evolution. Hortic Res. 2023; 10:uhad201

[84]

Liu JX, Feng K, Wang GL. et al. Elevated CO2 induces alteration in lignin accumulation in celery (Apium graveolens L.). Plant Physiol Biochem. 2018; 127:310-9

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