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Ploidy identification and chromosome-level genome assembly of Poa crymophila elucidate high-altitude adaptation

Xinyu Li1, 2, 3, Yubo Ma1, 3, Wenlin Li1, 3, Jihan Li1, 3, Mengjiao Li1, 3, Caixia Li1, Yan Wang1, Yi Yang2, Xinrong Ma1, 3#

1 China-Croatia "Belt and Road" Joint Laboratory on Biodiversity and Ecosystem Services, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China

2 College of Life Sciences, Sichuan University, Chengdu 610041, China

3 University of Chinese Academy of Sciences, Beijing 100049, China

 Highlights

• Poa crymophila is endemic to the Qinghai-Tibet Plateau with exceptional tolerance to environmental stresses.

• This study determined it has 28 chromosomes (2n=4x=28) and a 3.71 Gb autotetraploid genome.

• It diverged from its congeners 6.19–20.09 MYA, coinciding with Qinghai-Tibetan Plateau uplift.

• Stress-tolerance gene families expanded while photosynthesis-related families contracted.

• Abundant laccase and cytochrome genes offer potential for lignin and other secondary metabolites synthesis.

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摘要  

冷地早熟禾Poa crymophila),青藏高原特有的多年生禾,具有极强的寒旱适应性,是高原生态修复的先锋物种和优质牧草,具有重要的生态与经济价值。然而,受限于遗传背景不清,其极端环境适应机制难以深入解析。

本研究采用寡核苷酸荧光原位杂交(Oligo-FISH)技术,确定冷地早熟禾体细胞染色体数为2n= 28。结合二代 Illumina、三代 Pacbio HiFi Hi-C 测序策略,经 Genomescope Smudgeplot 分析,明确其为同源四倍体(2n= 4x = 28。通过从头组装获得大小为3.71 Gb的染色体级别参考基因组(单倍体约0.93 Gb;共注释出143,547高质量蛋白编码基因,BUSCO完整性达99.19%,LAI > 20,表明该基因组具有高度的完整性和准确性。

系统发育分析显示,冷地早熟禾与低矮早熟禾Poa infirma、仰卧早熟禾Poa supina)的分化发生 6.19–20.09 百万年前MYA与青藏高原快速抬升事件吻合,且早于大麦Hordeum和小麦Triticum)分化因此冷地早熟禾研究禾本科植物高海拔适应机制的理想模型。分化后,冷地早熟禾经历一次全基因组复制事件,这可能是形成同源四倍体的原因随后约在0.25 MYA发生一次以 Gypsy 为主的 LTR 大规模插入事件。比较基因组分析发现,其耐逆相关基因家族(如细胞色素 P450s、漆酶 LACs冷调控CORs 等)发生扩张,光合作用相关基因家族收缩;622个受到正向选择基因,富集于新陈代谢、应激和信号转导通路,包括抗氧化/解毒相关酶细胞色素氧化酶等,其中KMS1 在冷地早熟禾、青稞Hordeum vulgare var. nudum和西藏半野生小麦Triticum aestivum subsp. tibeticum中均正选择信号。此外,冷地早熟禾在旱寒胁迫下能合成大量具有保肝作用的次生代谢物五味子甲素(Schisandrin A)进一步提升了其作为牧草资源的价值。

综上,本研究揭示了冷地早熟禾通过基因组加倍、耐逆基因扩张、Gypsy-LTR  大规模插入及关键基因正选择等分子策略,协同驱动其获得高寒环境适应性,为耐逆牧草遗传改良及高海拔地区生态修复提供了宝贵的基因组资源。



Abstract  

Poa crymophila, a perennial Poaceae species native to the Qinghai-Tibet Plateau, exhibits remarkable adaptability to cold and drought. As a pioneer species for ecological restoration and a high-quality forage grass, it holds significant ecological and economic value. However, the lack of a clear genetic background has hindered in-depth investigation of its adaptative mechanisms. Here, Oligo-FISH analysis revealed that Poa crymophila possesses 28 chromosomes in its somatic cells (2n=28). De-novo genome assembly yielded a 3.71 Gb autotetraploid genome (2n=4x=28, monoploid size ≈0.93 Gb) with 143,547 annotated protein-coding genes. Phylogenetic analysis indicated that P. crymophila diverged from Poa infirma and Poa supina 6.19–20.09 million years ago, coinciding with the rapid uplift event of the Qinghai-Tibetan Plateau, after which a whole-genome duplication drove its autotetraploidy. Comparative genomics revealed expansions in stress-tolerance gene families (e.g., cytochrome P450slaccase LACs, Cold-Regulated CORs, etc.), and contractions in photosynthesis-related gene families. Additionally, 622 positively selected genes involved in metabolism, stress response and signaling were detected, including KMS1, which is shared with Tibetan Barley (Hordeum vulgare var. nudum) and Tibetan semi-wild wheat (Triticum aestivum subsp. tibeticum). Notably, P. crymophila could synthesize abundant schisandrin A under stress, a hepatoprotective secondary metabolite, further enhancing its value as a forage resource. These findings provide valuable genomic resources for breeding stress-tolerant forage crops and supporting ecological restoration in high-altitude regions.

Keywords:  Poa crymophila       Qinghai-Tibetan Plateau       Autotetraploid genome       Comparative genomics       Cold-drought adaptation       Stress-gene expansion       Schisandrin A  
Online: 12 September 2025  
Fund: 

This work was supported by the National Natural Science Foundation of China (31502003), the Sichuan Science & Technology Bureau Program, China (2024YFHZ0224 and 2024YFHZ0249) 

About author:  Xinyu Li, E-mail: lixinyu17@mails.ucas.edu.cn; Correspondence Xinrong Ma, E-mail: maxr@cib.ac.cn

Cite this article: 

Xinyu Li, Yubo Ma, Wenlin Li, Jihan Li, Mengjiao Li, Caixia Li, Yan Wang, Yi Yang, Xinrong Ma. 2025. Ploidy identification and chromosome-level genome assembly of Poa crymophila elucidate high-altitude adaptation. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.09.017

Agarwal P K, Gupta K, Lopato S, Agarwal P. 2017. Dehydration responsive element binding transcription factors and their applications for the engineering of stress tolerance. Journal of Experimental Botany68, 2135-2148.

Al Khateeb W M, Sher A A, Marcus J M, Schroeder D F. 2019. UVSSA, UBP12, and RDO2/TFIIS contribute to Arabidopsis UV tolerance. Frontiers in Plant Science10, 516.

Álvarez-Carretero S, Kapli P, Yang Z. 2023. Beginner’s guide on the use of PAML to detect positive selection. Molecular Biology And Evolution40, msad041.

Andargie M, Vinas M, Rathgeb A, Möller E, Karlovsky P. 2021. Lignans of Sesame (Sesamum indicum L.): A Comprehensive Review. Molecules (Basel, Switzerland)26(4), 883.

Babu V, Schumacher B. A C. 2016. A C. elegans homolog for the UV-hypersensitivity syndrome disease gene UVSSA. DNA Repair41, 8-15.

Bargmann B O, Laxalt A M, ter Riet B, van Schooten B, Merquiol E, Testerink C, Haring MA, Bartels D, Munnik T. 2009. Multiple PLDs required for high salinity and water deficit tolerance in plants. Plant & Cell Physiology50, 78-89.

Barr Z K, Werner T, Tilsner J. 2023. Heavy Metal-Associated Isoprenylated Plant Proteins (HIPPs) at Plasmodesmata: Exploring the Link between Localization and Function. Plants (Basel, Switzerland)12, 3015. 

Barth O, Vogt S, Uhlemann R, Zschiesche W, Humbeck K. 2009. Stress induced and nuclear localized HIPP26 from Arabidopsis thaliana interacts via its heavy metal associated domain with the drought stress related zinc finger transcription factor ATHB29. Plant Molecular Biology69, 213-226.

Benson C W, Sheltra M R, Maughan P J, Jellen E N, Robbins M D, Bushman B S, Patterson E L, Hall N D, Huff D R. 2023. Homoeologous evolution of the allotetraploid genome of Poa annua L. BMC Genomics24, 350.

Brands A, Ho T H. 2002. Function of a plant stress-induced gene, HVA22. Synthetic enhancement screen with its yeast homolog reveals its role in vesicular traffic. Plant Physiology130, 1121-1131.

Canturk F, Karaman M, Selby C P, Kemp M G, Kulaksiz-Erkmen G, Hu J, Li W, Lindsey-Boltz L A, Sancar A. 2016. Nucleotide excision repair by dual incisions in plants. Proceedings of the National Academy of Sciences of the United States of America113, 4706-4710.

Cardullo N, Pulvirenti L, Spatafora C, Musso N, Barresi V, Condorelli D F, Tringali C. 2016. Dihydrobenzofuran Neolignanamides: Laccase-Mediated Biomimetic Synthesis and Antiproliferative Activity. Journal of Natural Products79, 2122-2134.

Chakraborty P, Biswas A, Dey S, Bhattacharjee T, Chakrabarty S. 2023. Cytochrome P450 Gene Families: Role in Plant Secondary Metabolites Production and Plant Defense. Journal of Xenobiotics, 13, 402-423.

Chandra B R, Zhang J, Blum A, David H T H, Wu R, Nguyen H T. 2004. HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. Plant Science, 166, 855-862.

Chen C, Bai Y, Fang X, Guo H, Meng Q, Zhang W, Zhou P, Murodov A. 2019a. A Late Miocene Terrestrial Temperature History for the Northeastern Tibetan Plateau's Period of Tectonic Expansion. Geophysical Research Letters, 46, 8375-8386.

Chen E, Zhang X, Yang Z, Zhang C, Wang X, Ge X, Li F. 2019b. BR deficiency causes increased sensitivity to drought and yield penalty in cotton. BMC Plant Biology19, 220.

Chen J, Wang Z, Tan K, Huang W, Shi J, Li T, Hu J, Wang K, Wang C, Xin B, Zhao H, Song W, Hufford MB, Schnable JC, Jin W, Lai J. 2023. A complete telomere-to-telomere assembly of the maize genome. Nature Genetics55, 1221-1231.

Cheng H, Concepcion G T, Feng X, Zhang H, Li H. 2021. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nature Methods18, 170-175. 

Choi Y, Sims G E, Murphy S, Miller J R, Chan A P. 2012. Predicting the functional effect of amino acid substitutions and indels. PloS One7, e46688.

Cuadrado A, Golczyk H, Jouve N. 2009. A novel, simple and rapid nondenaturing FISH (ND-FISH) technique for the detection of plant telomeres. Potential used and possible target structures detected. Chromosome Research: An International Journal On The Molecular, Supramolecular And Evolutionary Aspects Of Chromosome Biology17, 755-762.

Davin L B, Wang H B, Crowell A L, Bedgar D L, Martin D M, Sarkanen S, Lewis N G. 1997. Stereoselective bimolecular phenoxy radical coupling by an auxiliary (dirigent) protein without an active center. Science (New York, N.Y.)275, 362-366.

Deng Y, Lin Y, Wei G, Hu X, Zheng Y, Ma J. 2024. Overexpression of the CpCOR413PM1 Gene from Wintersweet (Chimonanthus praecox) Enhances Cold and Drought Tolerance in Arabidopsis. Horticulturae, 10, 599.

Duan H, Schuler M A. 2005. Differential expression and evolution of the Arabidopsis CYP86A subfamily. Plant Physiology137, 1067-1081.

Emms D M, Kelly S. 2019. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biology20, 238.

Falev D I, Voronov I S, Onuchina A A, Faleva A V, Ul'yanovskii N V, Kosyakov D S. 2023. Analysis of Softwood Lignans by Comprehensive Two-Dimensional Liquid Chromatography. Molecules (Basel, Switzerland)28, 8114.

Fang S, Zhao P, Tan Z, Peng Y, Xu L, Jin Y, Wei F, Guo L, Yao X. 2022. Combining Physio-Biochemical Characterization and Transcriptome Analysis Reveal the Responses to Varying Degrees of Drought Stress in Brassica napus L. International Journal of Molecular Sciences23, 8555.

Flynn J M, Hubley R, Goubert C, Rosen J, Clark A G, Feschotte C, Smit A F. 2020. RepeatModeler2 for automated genomic discovery of transposable element families. Proceedings of the National Academy of Sciences of the United States of America117, 9451-9457. 

Frei D, Veekman E, Grogg D, Stoffel-Studer I, Morishima A, Shimizu-Inatsugi R, Yates S, Shimizu K K, Frey J E, Studer B, Copetti D. 2021. Ultralong Oxford Nanopore Reads Enable the Development of a Reference-Grade Perennial Ryegrass Genome Assembly. Genome Biology and Evolution13, evab159.

Gill S S, Peter Singh L, Gill R, Tuteja N. 2012. Generation and Scavenging of Reactive Oxygen Species in Plants under Stress. In Improving Crop Resistance to Abiotic Stress, 49-70. https://doi.org/10.1002/9783527632930.ch3.

Gomes Ferreira MD, Araújo Castro J, Santana Silva RJ, Micheli F. 2019. HVA22 from citrus: A small gene family whose some members are involved in plant response to abiotic stress. Plant Physiology and Biochemistry : PPB142, 395-404.

Grefen C, Blatt M R. 2008. SNAREs--molecular governors in signalling and development. Current Opinion in Plant Biology, 11, 600-609.

Gu H, Zhao Z, Wei Y, Li P, Lu Q, Liu Y, Wang T, Hu N, Wan S, Zhang B, Hu S, Peng R. 2023. Genome-Wide Identification and Functional Analysis of RF2 Gene Family and the Critical Role of GhRF2-32 in Response to Drought Stress in Cotton. Plants (Basel, Switzerland)12, 2613.

Guo M, Liu JH, Ma X, Luo DX, Gong ZH, Lu MH. 2016. The Plant Heat Stress Transcription Factors (HSFs): Structure, Regulation, and Function in Response to Abiotic Stresses. Frontiers in Plant Science7, 114. 

Guo W, Xin M, Wang Z, Yao Y, Hu Z, Song W, Yu K, Chen Y, Wang X, Guan P, Appels R, Peng H, Ni Z, Sun Q. 2020. Origin and adaptation to high altitude of Tibetan semi-wild wheat. Nature Communications11, 5085.

Guo X, Zhang L, Dong G, Xu Z, Li G, Liu N, Wang A, Zhu J. 2019. A novel cold-regulated protein isolated from Saussurea involucrata confers cold and drought tolerance in transgenic tobacco (Nicotiana tabacum). Plant science : An International Journal of Experimental Plant Biology289, 110246 .

HAN B, ZHANG P, ZHANG Z Q, WANG Y F, HU T M, YANG P Z J B. 2021. Molecular cloning and characterization of a novel gene MsKMS1 in Medicago sativa. Biologia Plantarum, 65, 1-9.

Hancke J L, Burgos R A, Ahumada F. 1999. Schisandra chinensis (Turcz.) Baill. Fitoterapia, 70, 451-471.

Hesse U. 2023. K-Mer-Based Genome Size Estimation in Theory and Practice. Methods in Molecular Biology (Clifton, N.J.)2672, 79-113.

Higa M, Tanaka K, Saijo M. 2018. Inhibition of UVSSA ubiquitination suppresses transcription-coupled nucleotide excision repair deficiency caused by dissociation from USP7. The FEBS Journal285, 965-976. 

Hoffmann N, Benske A, Betz H, Schuetz M, Samuels AL. 2020. Laccases and Peroxidases Co-Localize in Lignified Secondary Cell Walls throughout Stem Development. Plant Physiology, 184, 806-822.

Hou Z, Liang J, Cai X, Lin J, Wang X, Liu R, Lu L, Chai G, An C, Chen S, Qin Y, Zheng P. 2024. PeHVA22 gene family in passion fruit (Passiflora edulis): initial characterization and expression profiling diversity. Frontiers in Plant Science14, 1279001. 

Imran M, Ahmad N, Anjum FM, Khan MK, Mushtaq Z, Nadeem M, Hussain S. 2015. Potential protective properties of flax lignan secoisolariciresinol diglucoside. Nutrition Journal14, 71.

Janusz G, Pawlik A, Świderska-Burek U, Polak J, Sulej J, Jarosz-Wilkołazka A, Paszczyński A. 2020. Laccase Properties, Physiological Functions, and Evolution. International Journal of Molecular Sciences, 21,966.

Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A, Bridgland A, Meyer C, Kohl SAA, Ballard AJ, Cowie A, Romera-Paredes B, Nikolov S, Jain R, Adler J, Back T, Petersen S, Reiman D, Clancy E, Zielinski M, Steinegger M, Pacholska M, Berghammer T, Bodenstein S, Silver D, Vinyals O, Senior AW, Kavukcuoglu K, Kohli P, Hassabis D. 2021. Highly accurate protein structure prediction with AlphaFold. Nature, 596, 583-589.

Katagiri T, Takahashi S, Shinozaki K. 2001. Involvement of a novel Arabidopsis phospholipase D, AtPLDdelta, in dehydration-inducible accumulation of phosphatidic acid in stress signalling. The Plant Journal : for Cell and Molecular Biology26, 595-605.

Kirov I, Divashuk M, Van Laere K, Soloviev A, Khrustaleva L. 2014. An easy "SteamDrop" method for high quality plant chromosome preparation. Molecular Cytogenetics7, 21..

Kuo P, Henderson IR, Lambing C. 2022. CTAB DNA Extraction and Genotyping-by-Sequencing to Map Meiotic Crossovers in Plants. Methods in Molecular Biology (Clifton, N.J.)2484, 43-53.

Lewin H A, Larkin D M, Pontius J, O'Brien S J. 2009. Every genome sequence needs a good map. Genome Research19, 1925-1928.

Li L, Lavell A, Meng X, Berkowitz O, Selinski J, van de Meene A, Carrie C, Benning C, Whelan J, De Clercq I, Wang Y. 2019. Arabidopsis DGD1 SUPPRESSOR1 Is a Subunit of the Mitochondrial Contact Site and Cristae Organizing System and Affects Mitochondrial Biogenesis. The Plant Cell31, 1856-1878.

Li M, Hong Y, Wang X. 2009. Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochimica et Biophysica Acta1791, 927-935 .

Li Q, Yu HM, Meng XF, Lin JS, Li YJ, Hou BK. 2018a. Ectopic expression of glycosyltransferase UGT76E11 increases flavonoid accumulation and enhances abiotic stress tolerance in Arabidopsis. Plant Biology (Stuttgart, Germany)20, 10-19.

Li R T, Weng Z Y, Pu J X, Sun H D. 2008a. Chemical constituents from Schisandra sphenanthera. Chinese Chemical Letters, 19, 696-698..

Li S, Zheng H, Sui N, Zhang F. 2024. Class III peroxidase: An essential enzyme for enhancing plant physiological and developmental process by maintaining the ROS level: A review. A review. International Journal of Biological Macromolecules283, 137331.

Li W, Wang R, Li M, Li L, Wang C, Welti R, Wang X. 2008b. Differential degradation of extraplastidic and plastidic lipids during freezing and post-freezing recovery in Arabidopsis thalianaThe Journal of Biological Chemistry283, 461-468.

Li XY, Wang Y, Hou XY, Chen Y, Li CX, Ma XR. 2022. Flexible response and rapid recovery strategies of the plateau forage Poa crymophila to cold and drought. Frontiers in Plant Science13, 970496.

Li YJ, Li P, Wang T, Zhang FJ, Huang XX, Hou BK. 2018b. The maize secondary metabolism glycosyltransferase UFGT2 modifies flavonols and contributes to plant acclimation to abiotic stresses. Annals of Botany122, 1203-1217.

Liu Q Q, Lv L Y, He M H, Cai Z C, Shi J J. 2024. Screening of Suitable Mixed Grass Species and Seeding Rates of Four Native Grass Seeds in an Alpine Mining Area. Sustainability, 16, 17.

Liu X, Gong Q, Zhao C, Wang D, Ye X, Zheng G, Wang Y, Cao J, Sun C. 2023. Genome-wide analysis of cytochrome P450 genes in Citrus clementina and characterization of a CYP gene encoding flavonoid 3'-hydroxylase. Horticulture Research10, uhac283.

Marques JV, Kim KW, Lee C, Costa MA, May GD, Crow JA, Davin LB, Lewis NG. 2013. Next generation sequencing in predicting gene function in podophyllotoxin biosynthesis. The Journal of Biological Chemistry288, 466-479.

Marçais G, Kingsford C. 2011. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics (Oxford, England)27, 764-770.

Miao J, Feng Q, Li Y, Zhao Q, Zhou C, Lu H, Fan D, Yan J, Lu Y, Tian Q, Li W, Weng Q, Zhang L, Zhao Y, Huang T, Li L, Huang X, Sang T, Han B. 2021. Chromosome-scale assembly and analysis of biomass crop Miscanthus lutarioriparius genome. Nature Communications12, 2458.

Nguyen TX, Nguyen T, Alameldin H, Goheen B, Loescher W, Sticklen M. 2013a. Transgene Pyramiding of the HVA1 and mtlD in T3 Maize (Zea mays L.) Plants Confers Drought and Salt Tolerance, along with an Increase in Crop Biomass. International Journal of Agronomy598163, 10.

Nguyen T X, Sticklen M. 2013b. Barley HVA1 Gene Confers Drought and Salt Tolerance in Transgenic Maize (Zea Mays L.). Advances in Crop Science and Technology, 1, 105.

Ni X N, Guo W, Liu T, Li S H, Zhang J Z. 2023. Long-Term Effects of Altered Precipitation Patterns on Alpine Vegetation Species Composition on the Qinghai-Tibet Plateau. Forests, 14, 16.

Ono E, Nakai M, Fukui Y, Tomimori N, Fukuchi-Mizutani M, Saito M, Satake H, Tanaka T, Katsuta M, Umezawa T, Tanaka Y. 2006. Formation of two methylenedioxy bridges by a Sesamum CYP81Q protein yielding a furofuran lignan, (+)-sesamin. Proceedings of the National Academy of Sciences of the United States of America103, 10116-10121.

Ou S, Chen J, Jiang N. 2018. Assessing genome assembly quality using the LTR Assembly Index (LAI). Nucleic Acids Research46, e126.

Perales M, Eubel H, Heinemeyer J, Colaneri A, Zabaleta E, Braun HP. 2005. Disruption of a Nuclear Gene Encoding a Mitochondrial Gamma Carbonic Anhydrase Reduces Complex I and Supercomplex I+III2 Levels and Alters Mitochondrial Physiology in Arabidopsis. Journal of Molecular Biology350, 263-277.

Qi X, Tang X, Liu W, Fu X, Luo H, Ghimire S, Zhang N, Si H. 2020. A potato RING-finger protein gene StRFP2 is involved in drought tolerance. Plant Physiology and Biochemistry : PPB146, 438-446.

Ranallo-Benavidez TR, Jaron KS, Schatz MC. 2020. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nature Communications11, 1432.

Robbins MD, Bushman BS, Huff DR, Benson CW, Warnke SE, Maughan CA, Jellen EN, Johnson PG, Maughan PJ. 2023. Chromosome-Scale Genome Assembly and Annotation of Allotetraploid Annual Bluegrass (Poa annua L.). Genome Biology and Evolution15, evac180.

Rybnikář M, Šmejkal K, Žemlička M. 2019. Schisandra chinensis and its phytotherapeutical applications. Schisandra čínská a její využití ve fytoterapii. Ceska A Slovenska Farmacie : Casopis Ceske Farmaceuticke Spolecnosti A Slovenske Farmaceuticke Spolecnosti68, 95-118.

Samtani H, Sharma A, Khurana P. 2022. Overexpression of HVA1 Enhances Drought and Heat Stress Tolerance in Triticum aestivum Doubled Haploid Plants. Cells11, 912.

Schrodinger LLC. 2010. The PyMOL Molecular Graphics System, Version 1.3r1. Schrodinger, LLC, New York, 2010.

Shao HB, Liang ZS, Shao MA. 2005. LEA proteins in higher plants: structure, function, gene expression and regulation. Colloids Surf B Biointerfaces, 45,131-135.

Speckmann G J and Van Dijk G E. 1972. Chromosome number and plant morphology in some ecotypes of Poa pratensis L. Euphytica, 21, 171-180.

Sterjiades R, Dean JF, Eriksson KE. 1992. Laccase from Sycamore Maple (Acer pseudoplatanus) Polymerizes Monolignols. Plant Physiology99, 1162-1168.

Su C, Chen K, Ding Q, Mou Y, Yang R, Zhao M, Ma B, Xu Z, Ma Y, Pan Y, Chen M, Xi Y. 2018. Proteomic Analysis of the Function of a Novel Cold-Regulated Multispanning Transmembrane Protein COR413-PM1 in ArabidopsisInternational journal of molecular sciences19, 2572.

Sun J, Sheykh M, Windley BF, Talebian M, Cao M, Ahmadi N, Sha J. 2022. Magnetostratigraphic Age Control of the Timing of Tectonic Deformation and the Shifting Depositional Environments in the Dezful Embayment, Iran. Tectonics, 41, e2021TC006881.

Tarailo-Graovac M, Chen N. 2009. Using RepeatMasker to identify repetitive elements in genomic sequences. Current Protocols in BioinformaticsChapter 4, 4.10.1-4.10.14.

Thomashow M F. 1999. PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology50, 571-599.

Thornton LE, Peng H, Neff MM. 2011. Rice CYP734A cytochrome P450s inactivate brassinosteroids in Arabidopsis. Planta234, 1151-1162.

Vanholme R, Sundin L, Seetso KC, Kim H, Liu X, Li J, De Meester B, Hoengenaert L, Goeminne G, Morreel K, Haustraete J, Tsai HH, Schmidt W, Vanholme B, Ralph J, Boerjan W. 2019. COSY catalyses trans-cis isomerization and lactonization in the biosynthesis of coumarins. Nature Plants5, 1066-1075. 

Villarreal F, Martín V, Colaneri A, González-Schain N, Perales M, Martín M, Lombardo C, Braun HP, Bartoli C, Zabaleta E. 2009. Ectopic expression of mitochondrial gamma carbonic anhydrase 2 causes male sterility by anther indehiscence. Plant Molecular Biology70, 471-485.

Vurture GW, Sedlazeck FJ, Nattestad M, Underwood CJ, Fang H, Gurtowski J, Schatz MC. 2017. GenomeScope: fast reference-free genome profiling from short reads. Bioinformatics (Oxford, England)33, 2202-2204.

Wang J, Lian L, Qi J, Fang Y, Nyporko A, Yu Q, Bai L, Pan L. 2023a. Metabolic resistance to acetolactate synthase inhibitors in Beckmannia syzigachne: identification of CYP81Q32 and its transcription regulation. The Plant Journal : for Cell and Molecular Biology115, 317-334.

Wang M, Wang L, Yu X, Zhao J, Tian Z, Liu X, Wang G, Zhang L, Guo X. 2023b. Enhancing cold and drought tolerance in cotton: a protective role of SikCOR413PM1. BMC Plant Biology, 23, 577.

Wang X, Devaiah S P, Zhang W, Welti R. 2006. Signaling functions of phosphatidic acid. Progress in Lipid Research, 45, 250-278.

Wang Y, Li X Y, Li C X, He Y, Hou X Y, Ma X R. 2021. The Regulation of Adaptation to Cold and Drought Stresses in Poa crymophila Keng Revealed by Integrative Transcriptomics and Metabolomics Analysis. Frontiers in Plant Science12, 631117.

Wang Y, Tang H, Debarry J D, Tan X, Li J, Wang X, Lee T H, Jin H, Marler B, Guo H, Kissinger J C, Paterson A H. 2012. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research40, e49.

Wu T, Hu E, Xu S, Chen M, Guo P, Dai Z, Feng T, Zhou L, Tang W, Zhan L, Fu X, Liu S, Bo X, Yu G. 2021. clusterProfiler 4.0: A universal enrichment tool for interpreting omics data. Innovation (Cambridge (Mass.))2, 100141.

Xie T, Liu Z, Wang G. 2020. Structural basis for monolignol oxidation by a maize laccase. Nature Plants6, 231-237. 

Yan C, Li XN, Peng ZL, Wu W, Wang Z, Zhu ZR, Liu JC, Wang Y, Ren JL, Zhang ZY, Li JT. 2025. Hologenomics Reveals Specialized Dietary Adaptations in the Mengla Snail-Eating Snake. Advanced Science (Weinheim, Baden-Wurttemberg, Germany), 16, e09999.

Yang N, Liu B, Yang P, Chen X, Li H, Wang W, Li Q, Wang S. 2021. Molecular cloning, characterization and expression analysis of CbPLDδ gene from Chorispora bungeana in low temperature. Cryobiology98, 119-126.

Yang Z, He F, Mai Y, Fan S, An Y, Li K, Wu F, Tang M, Yu H, Liu JX, Xia R. 2024. A near-complete assembly of the Houttuynia cordata genome provides insights into the regulatory mechanism of flavonoid biosynthesis in Yuxingcao. Plant Communications5, 101075.

Yao X, Wu K, Yao Y, Li J, Ren Y, Chi D. 2017. The response mechanism of the HVA1 gene in hulless barley under drought stress. Italian Journal of Agronomy, 12, 804.

Ying S, Scheible WR, Lundquist PK. 2023. A stress-inducible protein regulates drought tolerance and flowering time in Brachypodium and Arabidopsis. Plant Physiology191, 643-659.

Zeng X, Long H, Wang Z, Zhao S, Tang Y, Huang Z, Wang Y, Xu Q, Mao L, Deng G, Yao X, Li X, Bai L, Yuan H, Pan Z, Liu R, Chen X, WangMu Q, Chen M, Yu L, Liang J, DunZhu D, Zheng Y, Yu S, LuoBu Z, Guang X, Li J, Deng C, Hu W, Chen C, TaBa X, Gao L, Lv X, Abu YB, Fang X, Nevo E, Yu M, Wang J, Tashi N. 2015. The draft genome of Tibetan hulless barley reveals adaptive patterns to the high stressful Tibetan Plateau. Proceedings of the National Academy of Sciences of the United States of America112, 1095-1100.

Zeng X, Xu T, Ling Z, Wang Y, Li X, Xu S, Xu Q, Zha S, Qimei W, Basang Y, Dunzhu J, Yu M, Yuan H, Nyima T. 2020. An improved high-quality genome assembly and annotation of Tibetan hulless barley. Scientific Data7, 139.

Zhang B, Wang H, Zhang Y. 2020. SNARE proteins and their role in plant ion channel regulation. Plant Growth Regulation, 92, 443-453.

Zhang KL, Leng YN, Hao RR, Zhang WY, Li HF, Chen MX, Zhu FY. 2024. Adaptation of High-Altitude Plants to Harsh Environments: Application of Phenotypic-Variation-Related Methods and Multi-Omics Techniques. International Journal of Molecular Sciences25, 12666.

Zhang X, Zhang S, Zhao Q, Ming R, Tang H. 2019. Assembly of allele-aware, chromosomal-scale autopolyploid genomes based on Hi-C data. Nature Plants5, 833-845. 

Zhao L, Wang B, Yang T, Yan H, Yu Q, Wang J. 2023. Genome-wide identification and analysis of the evolution and expression pattern of the HVA22 gene family in three wild species of tomatoes. PeerJ11, e14844.

Zhao Q, Nakashima J, Chen F, Yin Y, Fu C, Yun J, Shao H, Wang X, Wang ZY, Dixon RA. 2013. Laccase is necessary and nonredundant with peroxidase for lignin polymerization during vascular development in Arabidopsis. The Plant Cell25, 3976-3987. 

Zhou X, Hua D, Chen Z, Zhou Z, Gong Z. 2009. Elongator mediates ABA responses, oxidative stress resistance and anthocyanin biosynthesis in Arabidopsis. The Plant Journal : for Cell and Molecular Biology60, 79-90.

Zhu T, Wang L, Rimbert H, Rodriguez JC, Deal KR, De Oliveira R, Choulet F, Keeble-Gagnère G, Tibbits J, Rogers J, Eversole K, Appels R, Gu YQ, Mascher M, Dvorak J, Luo MC. 2021. Optical maps refine the bread wheat Triticum aestivum cv. Chinese Spring genome assembly. The Plant Journal : for Cell and Molecular Biology107, 303-314.

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