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A high-quality genome sequence of alkaligrass provides insights into halophyte stress tolerance

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Abstract

Alkaligrass (Puccinellia tenuiflora) is a monocotyledonous halophytic forage grass widely distributed in Northern China. It belongs to the Gramineae family and shares a close phylogenetic relationship with the cereal crops, wheat and barley. Here, we present a high-quality chromosome-level genome sequence of alkaligrass assembled from Illumina, PacBio and 10× Genomics reads combined with genome-wide chromosome conformation capture (Hi-C) data. The ∼1.50 Gb assembled alkaligrass genome encodes 38,387 protein-coding genes, and 54.9% of the assembly are transposable elements, with long terminal repeats being the most abundant. Comparative genomic analysis coupled with stress-treated transcriptome profiling uncovers a set of unique saline- and alkaline-responsive genes in alkaligrass. The high-quality genome assembly and the identified stress related genes in alkaligrass provide an important resource for evolutionary genomic studies in Gramineae and facilitate further understanding of molecular mechanisms underlying stress tolerance in monocotyledonous halophytes. The alkaligrass genome data is freely available at http://xhhuanglab.cn/data/alkaligrass.html.

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Data availability

The assembled alkaligrass genome has been deposited in BIGD under Bioproject number PRJCA002121. The genome assembly and gene annotations of alkaligrass can also be accessed from http://www.xhhuanglab.cn/data/alkaligrass.html.

References

  • Ardie, S.W., Xie, L., Takahashi, R., Liu, S., and Takano, T. (2009). Cloning of a high-affinity K+ transporter gene PutHKT2;1 from Puccinellia tenuiflora and its functional comparison with OsHKT2;1 from rice in yeast and Arabidopsis. J Exp Bot 60, 3491–3502.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ardie, S.W., Liu, S., and Takano, T. (2010). Expression of the AKT1-type K+ channel gene from Puccinellia tenuiflora, PutAKT1, enhances salt tolerance in Arabidopsis. Plant Cell Rep 29, 865–874.

    Article  CAS  PubMed  Google Scholar 

  • Buchfink, B., Xie, C., and Huson, D.H. (2015). Fast and sensitive protein alignment using diamond. Nat Methods 12, 59–60.

    Article  CAS  PubMed  Google Scholar 

  • Burton, J.N., Adey, A., Patwardhan, R.P., Qiu, R., Kitzman, J.O., and Shendure, J. (2013). Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat Biotechnol 31, 1119–1125.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chin, C.S., Peluso, P., Sedlazeck, F.J., Nattestad, M., Concepcion, G.T., Clum, A., Dunn, C., O’Malley, R., Figueroa-Balderas, R., Morales-Cruz, A., et al. (2016). Phased diploid genome assembly with single-molecule real-time sequencing. Nat Methods 13, 1050–1054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chin, C.S., Alexander, D.H., Marks, P., Klammer, A.A., Drake, J., Heiner, C., Clum, A., Copeland, A., Huddleston, J., Eichler, E.E., et al. (2013). Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10, 563–569.

    Article  CAS  PubMed  Google Scholar 

  • Colmer, T.D., Munns, R., and Flowers, T.J. (2005). Improving salt tolerance of wheat and barley: future prospects. Aust J Exp Agric 45, 1425–1443.

    Article  CAS  Google Scholar 

  • Coombe, L., Zhang, J., Vandervalk, B.P., Chu, J., Jackman, S.D., Birol, I., and Warren, R.L. (2018). ARKS: chromosome-scale scaffolding of human genome drafts with linked read kmers. BMC Bioinformatics 19, 234.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dassanayake, M., Oh, D.H., Haas, J.S., Hernandez, A., Hong, H., Ali, S., Yun, D.J., Bressan, R.A., Zhu, J.K., Bohnert, H.J., et al. (2011). The genome of the extremophile crucifer Thellungiella parvula. Nat Genet 43, 913–918.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dolezel, J., Greilhuber, J., and Suda, J. (2007). Estimation of nuclear DNA content in plants using flow cytometry. Nat Protoc 2, 2233–2244.

    Article  CAS  PubMed  Google Scholar 

  • Ellinghaus, D., Kurtz, S., and Willhoeft, U. (2008). Ltrharvest, an efficient and flexible software for de novo detection ofltr retrotransposons. BMC Bioinformatics 9, 18.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Emms, D.M., and Kelly, S. (2015). OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16, 157.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Feng, W., Kita, D., Peaucelle, A., Cartwright, H.N., Doan, V., Duan, Q., Liu, M.C., Maman, J., Steinhorst, L., Schmitz-Thom, I., et al. (2018). The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr Biol 28, 666–675.e5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., et al. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29, 644–652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grant, C.E., Bailey, T.L., and Noble, W.S. (2011). FIMO: Scanning for occurrences of a given motif. Bioinformatics 27, 1017–1018.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan, Q., Wang, Z., Wang, X., Takano, T., and Liu, S. (2015). A peroxisomal APX from Puccinellia tenuiflora improves the abiotic stress tolerance of transgenic Arabidopsis thaliana through decreasing of H2O2 accumulation. J Plant Physiol 175, 183–191.

    Article  CAS  PubMed  Google Scholar 

  • Guo, L.Q., Shi, D.C., and Wang, D.L. (2010). The key physiological response to alkali stress by the alkali-resistant halophyte Puccinellia tenuiflora is the accumulation of large quantities of organic acids and into the rhyzosphere. J Agron Crop Sci 196, 123–135.

    Article  CAS  Google Scholar 

  • Han, M.V., Thomas, G.W.C., Lugo-Martinez, J., and Hahn, M.W. (2013). Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3. Mol Biol Evol 30, 1987–1997.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones, P., Binns, D., Chang, H.Y., Fraser, M., Li, W., McAnulla, C., McWilliam, H., Maslen, J., Mitchell, A., Nuka, G., et al. (2014). InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh, K., Misawa, K., Kuma, K., and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30, 3059–3066.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kielbasa, S.M., Wan, R., Sato, K., Horton, P., and Frith, M.C. (2011). Adaptive seeds tame genomic sequence comparison. Genome Res 21, 487–493.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, D., Langmead, B., and Salzberg, S.L. (2015). HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12, 357–360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi, S., Abe, N., Yoshida, K.T., Liu, S., and Takano, T. (2012). Molecular cloning and characterization of plasma membrane- and vacuolar-type Na+/H+ antiporters of an alkaline-salt-tolerant monocot, Puccinellia tenuiflora. J Plant Res 125, 587–594.

    Article  CAS  PubMed  Google Scholar 

  • Koce, J.D., Škondrić, S., Bačič, T., and Dermastia, M. (2008). Amounts of nuclear DNA in marine halophytes. Aquat Bot 89, 385–389.

    Article  CAS  Google Scholar 

  • Konopka-Postupolska, D., Clark, G., Goch, G., Debski, J., Floras, K., Cantero, A., Fijolek, B., Roux, S., and Hennig, J. (2009). The role of annexin 1 in drought stress in Arabidopsis. Plant Physiol 150, 1394–1410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korf, I. (2004). Gene finding in novel genomes. BMC Bioinformatics 5, 59.

    Article  PubMed  PubMed Central  Google Scholar 

  • Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S.J., and Marra, M.A. (2009). Circos: an information aesthetic for comparative genomics. Genome Res 19, 1639–1645.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, Y.P., Giorgi, F.M., Lohse, M., Kvederaviciute, K., Klages, S., Usadel, B., Meskiene, I., Reinhardt, R., and Hincha, D.K. (2013). Transcriptome sequencing and microarray design for functional genomics in the extremophile Arabidopsis relative Thellungiella salsuginea (Eutrema salsugineum). BMC Genomics 14, 793.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, C., Yeh, F.L., Cheung, A.Y., Duan, Q., Kita, D., Liu, M.C., Maman, J., Luu, E.J., Wu, B.W., Gates, L., et al. (2015). Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. eLife 4, e06587.

    Article  PubMed Central  Google Scholar 

  • Liu, H., Zhang, X., Takano, T., and Liu, S. (2009). Characterization of a PutCAX1 gene from Puccinellia tenuiflora that confers Ca2+ and Ba2+ tolerance in yeast. Biochem Biophys Res Commun 383, 392–396.

    Article  CAS  PubMed  Google Scholar 

  • Lomsadze, A., Burns, P.D., and Borodovsky, M. (2014). Integration of mapped RNA-Seq reads into automatic training of eukaryotic gene finding algorithm. Nucleic Acids Res 42, e119.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lv, B.S.., Li, X.W., Ma, H.Y., Sun, Y., Wei, L.X., Jiang, C.J., and Liang, Z. W. (2013). Differences in growth and physiology of rice in response to different saline-alkaline stress factors. Agron J 105, 1119–1128.

    Article  CAS  Google Scholar 

  • Lynch, M., and Conery, J.S. (2000). The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155.

    Article  CAS  PubMed  Google Scholar 

  • Ma, X., and Cao, X. (2018). Cotton variant genomes—a breakthrough in population genetics analysis. Sci China Life Sci 61, 869–870.

    Article  PubMed  Google Scholar 

  • Mahajan, S., and Tuteja, N. (2005). Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444, 139–158.

    Article  CAS  PubMed  Google Scholar 

  • Mayer, K.F.X., Waugh, R., Brown, J.W.S., Schulman, A., Langridge, P., Platzer, M., Fincher, G.B., Muehlbauer, G.J., Sato, K., Close, T.J., et al. (2012). A physical, genetic and functional sequence assembly of the barley genome. Nature 491, 711–716.

    Article  CAS  PubMed  Google Scholar 

  • Meng, X., Zhao, Q., Jin, Y., Yu, J., Yin, Z., Chen, S., and Dai, S. (2016). Chilling-responsive mechanisms in halophyte Puccinellia tenuiflora seedlings revealed from proteomics analysis. J Proteomics 143, 365–381.

    Article  CAS  PubMed  Google Scholar 

  • Mondal, T.K., Rawal, H.C., Chowrasia, S., Varshney, D., Panda, A.K., Mazumdar, A., Kaur, H., Gaikwad, K., Sharma, T.R., and Singh, N.K. (2018). Draft genome sequence of first monocot-halophytic species Oryza coarctata reveals stress-specific genes. Sci Rep 8, 13698.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Murray, B.G., De Lange, P.J., and Ferguson, A.R. (2005). Nuclear DNA variation, chromosome numbers and polyploidy in the endemic and indigenous grass flora of New Zealand. Ann Bot 96, 1293–1305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oh, D.H., Dassanayake, M., Haas, J.S., Kropornika, A., Wright, C., d’Urzo, M.P., Hong, H., Ali, S., Hernandez, A., Lambert, G.M., et al. (2010). Genome structures and halophyte-specific gene expression of the extremophile Thellungiella parvula in comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis. Plant Physiol 154, 1040–1052.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ou, S., and Jiang, N. (2019). Ltr_finder_parallel: Parallelization of ltrfinder enabling rapid identification of long terminal repeat retrotransposons. Mobile DNA 10, 48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ou, S., and Jiang, N. (2018). Ltr_retriever: A highly accurate and sensitive program for identification of long terminal repeat retrotransposons. Plant Physiol 176, 1410–1422.

    Article  CAS  PubMed  Google Scholar 

  • Peng, Y.H., Zhu, Y.F., Mao, Y.Q., Wang, S.M., Su, W.A., and Tang, Z.C. (2004). Alkali grass resists salt stress through high [K+] and an endodermis barrier to Na+. J Exp Bot 55, 939–949.

    Article  CAS  PubMed  Google Scholar 

  • Pertea, M., Pertea, G.M., Antonescu, C.M., Chang, T.C., Mendell, J.T., and Salzberg, S.L. (2015). StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33, 290–295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rambaut, A. (2009). FigTree 1.3. http://tree.bio.ed.ac.uk/software/figtree/.

  • Salamov, A.A., and Solovyev, V.V. (2000). Ab initio gene finding in Drosophila genomic DNA. Genome Res 10, 516–522.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen, Q., Bourdais, G., Pan, H., Robatzek, S., and Tang, D. (2017). Arabidopsis glycosylphosphatidylinositol-anchored protein LLG1 associates with and modulates FLS2 to regulate innate immunity. Proc Natl Acad Sci USA 114, 5749–5754.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen, Y., Du, H., Liu, Y., Ni, L., Wang, Z., Liang, C., and Tian, Z. (2019). Update soybean Zhonghuang 13 genome to a golden reference. Sci China Life Sci 62, 1257–1260.

    Article  PubMed  Google Scholar 

  • Shi, D., Yin, S., Yang, G., and Zhao, K. (2002). Citric acid accumulation in an alkali-tolerant plant Puccinellia tenuiflora under alkaline stress. Acta Bot Sin 44, 537–540.

    CAS  Google Scholar 

  • Simão, F.A., Waterhouse, R.M., Ioannidis, P., Kriventseva, E.V., and Zdobnov, E.M. (2015). BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212.

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanke, M., Schöffmann, O., Morgenstern, B., and Waack, S. (2006). Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources. BMC Bioinformatics 7, 62.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sun, G., Peng, Y., Shao, H., Chu, L., Zhao, X., Min, H., Cao, W., and Wei, C. (2005). Does Puccinelia tenuiflora have the ability of salt exudation? Colloids Surf B Biointerfaces 46, 197–203.

    Article  CAS  Google Scholar 

  • Suo, J., Zhang, H., Zhao, Q., Zhang, N., Zhang, Y., Li, Y., Song, B., Yu, J., Cao, J., Wang, T., et al. (2019). Na2CO3-responsive photosynthetic and ROS scavenging mechanisms in chloroplasts of alkaligrass revealed by phosphoproteomics. bioRxiv 871046.

  • Tang, H., Zhang, X., Miao, C., Zhang, J., Ming, R., Schnable, J.C., Schnable, P.S., Lyons, E., and Lu, J. (2015). ALLMAPS: robust scaffold ordering based on multiple maps. Genome Biol 16, 3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang, H., Wang, X., Bowers, J.E., Ming, R., Alam, M., and Paterson, A.H. (2008). Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res 18, 1944–1954.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tarailo-Graovac, M., and Chen, N. (2009). Using RepeatMasker to identify repetitive elements in genomic sequences. Curr Protocols BioInf 25, 4–10.

    Article  Google Scholar 

  • Tuteja, N. (2007). Mechanisms of high salinity tolerance in plants. Methods Enzymol 428, 419–438.

    Article  CAS  PubMed  Google Scholar 

  • International Brachypodium Initiative. (2010). Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463, 763–768.

    Article  CAS  Google Scholar 

  • Walker, B.J., Abeel, T., Shea, T., Priest, M., Abouelliel, A., Sakthikumar, S., Cuomo, C.A., Zeng, Q., Wortman, J., Young, S.K., et al. (2014). Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang, C.M., Zhang, J.L., Liu, X.S., Li, Z., Wu, G.Q., Cai, J.Y., Flowers, T. J., and Wang, S.M. (2009). Puccinellia tenuiflora maintains a low Na+ level under salinity by limiting unidirectional Na+ influx resulting in a high selectivity for K+ over Na+. Plant Cell Environ 32, 486–496.

    Article  CAS  PubMed  Google Scholar 

  • Wang, L., Ma, G., Wang, H., Cheng, C., Mu, S., Quan, W., Jiang, L., Zhao, Z., Zhang, Y., Zhang, K., et al. (2019). A draft genome assembly of halophyte Suaeda aralocaspica, a plant that performs C4 photosynthesis within individual cells. GigaScience 8, giz116.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang, X., Ma, X., Wang, H., Li, B., Clark, G., Guo, Y., Roux, S., Sun, D., and Tang, W. (2015). Proteomic study ofmicrosomal proteins reveals a key role for Arabidopsis Annexin 1 in mediating heat stress-induced increase in intracellular calcium levels. Mol Cell Proteomics 14, 686–694.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Y., Chu, Y., Liu, G., Wang, M.H., Jiang, J., Hou, Y., Qu, G., and Yang, C. (2007). Identification of expressed sequence tags in an alkali grass (Puccinellia tenuiflora) cDNA library. J Plant Physiol 164, 78–89.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Yang, C., Liu, G., and Jiang, J. (2007). Development of a cDNA microarray to identify gene expression of Puccinellia tenuiflora under saline-alkali stress. Plant Physiol Biochem 45, 567–576.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Tang, H., Debarry, J.D., Tan, X., Li, J., Wang, X., Lee, T., Jin, H., Marler, B., Guo, H., et al. (2012). MCScanX: Atoolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40, e49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warren, R.L., Yang, C., Vandervalk, B.P., Behsaz, B., Lagman, A., Jones, S.J.M., and Birol, I. (2015). LINKS: Scalable, alignment-free scaffolding of draft genomes with long reads. GigaScience 4, 35.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu, H.J., Zhang, Z., Wang, J.Y., Oh, D.H., Dassanayake, M., Liu, B., Huang, Q., Sun, H.X., Xia, R., Wu, Y., et al. (2012). Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc Natl Acad Sci USA 109, 12219–12224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu, Z., and Wang, H. (2007). Ltrfinder: An efficient tool for the prediction of full-length ltr retrotransposons. Nucleic Acids Res 35, W265–W268.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang, R., Jarvis, D.E., Chen, H., Beilstein, M.A., Grimwood, J., Jenkins, J., Shu, S.Q., Prochnik, S., Xin, M., Ma, C., et al. (2013). The reference genome of the halophytic plant Eutrema salsugineum. Front Plant Sci 4, 46.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yin, Z., Zhang, H., Zhao, Q., Yoo, M.J., Zhu, N., Yu, J., Yu, J., Guo, S., Miao, Y., Chen, S., et al. (2019). Physiological and comparative proteomic analyses of saline-alkali NaHCO3-responses in leaves of halophyte Puccinellia tenuiflora. Plant Soil 437, 137–158.

    Article  CAS  Google Scholar 

  • Yu, J., Chen, S., Wang, T., Sun, G., and Dai, S. (2013). Comparative proteomic analysis of Puccinellia tenuiflora leaves under Na2CO3 stress. Int J Mol Sci 14, 1740–1762.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, J., Chen, S., Zhao, Q., Wang, T., Yang, C., Diaz, C., Sun, G., and Dai, S. (2011). Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora. J Proteome Res 10, 3852–3870.

    Article  CAS  PubMed  Google Scholar 

  • Yu, Y., and Assmann, S.M. (2018). Inter-relationships between the heterotrimeric Gβ subunit AGB1, the receptor-like kinase FERONIA, and RALF1 in salinity response. Plant Cell Environ 41, 2475–2489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, C.Q., Nishiuchi, S., Liu, S., and Takano, T. (2008). Characterization of two plasma membrane protein 3 genes (PutPMP3) from the alkali grass, Puccinellia tenuiflora, and functional comparison of the rice homologues, OsLti6a/b from rice. BMB Rep 41, 448–454.

    Article  Google Scholar 

  • Zhang, H., Han, B., Wang, T., Chen, S., Li, H., Zhang, Y., and Dai, S. (2012). Mechanisms of plant salt response: insights from proteomics. J Proteome Res 11, 49–67.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, H., Huang, L., Hong, Y., and Song, F. (2016). BOTRYTIS-INDUCED KINASE1, a plasma membrane-localized receptor-like protein kinase, is a negative regulator of phosphate homeostasis in Arabidopsis thaliana. BMC Plant Biol 16, 152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, M., Takano, T., Liu, S., and Zhang, X. (2014). Abiotic stress response in yeast and metal-binding ability ofa type 2 metallothionein-like protein (PutMT2) from Puccinellia tenuiflora. Mol Biol Rep 41, 5839–5849.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, X., Wei, L., Wang, Z., and Wang, T. (2013). Physiological and molecular features of Puccinellia tenuiflora tolerating salt and alkaline-salt stress. J Integrat Plant Biol 55, 262–276.

    Article  CAS  Google Scholar 

  • Zhang, Y., Zhang, Y., Yu, J., Zhang, H., Wang, L., Wang, S., Guo, S., Miao, Y., Chen, S., Li, Y., et al. (2019). NaCl-responsive ROS scavenging and energy supply in alkaligrass callus revealed from proteomic analysis. BMC Genomics 20, 990.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, C., Zayed, O., Yu, Z., Jiang, W., Zhu, P., Hsu, C.C., Zhang, L., Tao, W.A., Lozano-Durán, R., and Zhu, J.K. (2018). Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis. Proc Natl Acad Sci USA 115, 13123–13128.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, Q., Feng, Q., Lu, H., Li, Y., Wang, A., Tian, Q., Zhan, Q., Lu, Y., Zhang, L., Huang, T., et al. (2018). Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat Genet 50, 278–284.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, Q., Suo, J., Chen, S., Jin, Y., Ma, X., Yin, Z., Zhang, Y., Wang, T., Luo, J., Jin, W., et al. (2016). Na2CO3-responsive mechanisms in halophyte Puccinellia tenuiflora roots revealed by physiological and proteomic analyses. Sci Rep 6, 32717.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, J.K. (2016). Abiotic stress signaling and responses in plants. Cell 167, 313–324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank Dr. Zhangjun Fei from Cornell University for critical reading and editing of the manuscript. This work was supported by grants from the National Key Research and Development Program of China (2018YFA090060), the Foundation of Shanghai Science and Technology Committee (17391900600), the Fund of Shanghai Engineering Research Center of Plant Germplasm Resources (17DZ2252700), and the Natural Science Foundation of Heilongjiang Province (ZD2019C003).

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  1. Contributed equally to this work

Authors and Affiliations

  1. Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, 200234, China

    Wenting Zhang, Jie Liu, Yongxue Zhang, Jie Qiu, Fenhong Hu, Shaojun Dai & Xuehui Huang

  2. Key Laboratory of Saline-alkali Vegetation Ecology Restoration (Northeast Forestry University), Ministry of Education, College of Life Sciences, Northeast Forestry University, Harbin, 150040, China

    Yongxue Zhang, Ying Li & Baojiang Zheng

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  1. Wenting Zhang
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  2. Jie Liu
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Correspondence to Fenhong Hu, Shaojun Dai or Xuehui Huang.

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Figure S1 Morphology of alkaligrass.

Figure S2 Genome size estimation in alkaligrass by flow cytometry.

Figure S3 Genome size estimation by K-mer analysis.

Figure S4 Hi-C map of the alkaligrass genome showing genome-wide chromatin interactions.

Figure S5 Integrated work-flow for the assembly of the alkaligrass genome.

Figure S6 Insertion time of (A) intact LTRs, (B) Copia/LTRs and (C) Gypsy/LTRs in seven BOP species.

Figure S7 Phylogenetic tree of the most expanded family (F-box/FBD/LRR-repeat protein) in alkaligrass.

Figure S8 Comparative genomic analysis.

Supplemental File 1. Abbreviations of the protein names in the pathways in Figure 4C.

Supplemental File 2 FIMO analysis result of four FER’s promoter sequence.

Supplemental File 3. The primer sequences of the alkaligrass genes for qRT-PCR

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Zhang, W., Liu, J., Zhang, Y. et al. A high-quality genome sequence of alkaligrass provides insights into halophyte stress tolerance. Sci. China Life Sci. 63, 1269–1282 (2020). https://doi.org/10.1007/s11427-020-1662-x

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  • DOI: https://doi.org/10.1007/s11427-020-1662-x

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