The genome of the recretohalophyte Limonium bicolor provides insights into salt gland development and salinity adaptation during terrestrial evolution

Molecular Plant - Tập 15 - Trang 1024-1044 - 2022
Fang Yuan1, Xi Wang1, Boqing Zhao1, Xiaojing Xu1, Miao Shi2, Bingying Leng1, Xinxiu Dong1, Chaoxia Lu1, Zhongtao Feng1, Jianrong Guo1, Guoliang Han1, Haikuan Zhang2, Jianwei Huang2, Min Chen1, Bao-Shan Wang1
1Shandong Provincial Key Laboratory of Plant Stress, College of Life Sciences, Shandong Normal University, Ji’nan, Shandong, China
2Berry Genomics Corporation, Beijing, China

Tài liệu tham khảo

Arisz, 1955, The secretion of the salt glands of Limonium latifolium Ktze, Acta Bot. Neerl., 4, 322, 10.1111/j.1438-8677.1955.tb00334.x Badouin, 2017, The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution, Nature, 546, 148, 10.1038/nature22380 Bernhardt, 2003, The bHLH genes GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root, Development, 130, 6431, 10.1242/dev.00880 Berthomieu, 2003, Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance, EMBO J., 22, 2004, 10.1093/emboj/cdg207 Butts, 2016, Novel proteases from the genome of the carnivorous plant Drosera capensis: structural prediction and comparative analysis, Proteins, 84, 1517, 10.1002/prot.25095 Canales, 2017, Nitrate induction of root hair density is mediated by TGA1/TGA4 and CPC transcription factors in Arabidopsis thaliana, Plant J., 92, 305, 10.1111/tpj.13656 Caperta, 2020, Secretory structures in plants: lessons from the Plumbaginaceae on their origin, evolution and roles in stress tolerance, Plant Cell Environ., 43, 2912, 10.1111/pce.13825 Chater, 2017, Origins and evolution of stomatal development, Plant Physiol., 174, 624, 10.1104/pp.17.00183 Chaves, 2008, Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell, Ann. Bot., 103, 551, 10.1093/aob/mcn125 Chin, 2016, Phased diploid genome assembly with single-molecule real-time sequencing, Nat. Methods, 13, 1050, 10.1038/nmeth.4035 Chopra, 2019, Genetic and molecular analysis of trichome development in Arabis alpina, Proc. Natl. Acad. Sci. U S A, 116, 12078, 10.1073/pnas.1819440116 Clough, 2010, Floral dip: a simplified method for Agrobacterium -mediated transformation of Arabidopsis thaliana, Plant J., 16, 735, 10.1046/j.1365-313x.1998.00343.x Copetti, 2017, Extensive gene tree discordance and hemiplasy shaped the genomes of North American columnar cacti, Proc. Natl. Acad. Sci. U S A, 114, 12003, 10.1073/pnas.1706367114 Criscuolo, 2011, morePhyML: improving the phylogenetic tree space exploration with PhyML 3, Mol. Phylogenet. Evol., 61, 944, 10.1016/j.ympev.2011.08.029 Dohm, 2014, The genome of the recently domesticated crop plant sugar beet (Beta vulgaris), Nature, 505, 546, 10.1038/nature12817 Dolan, 2001, Evolution and genetics of root hair stripes in the root epidermis, J. Exp. Bot., 52, 413, 10.1093/jexbot/52.suppl_1.413 Doroshkov, 2019, The evolution of gene regulatory networks controlling Arabidopsis thaliana L. trichome development, BMC Plant Biol., 19, 53, 10.1186/s12870-019-1640-2 Du, 2019, Assembly of chromosome-scale contigs by efficiently resolving repetitive sequences with long reads, Nat. Commun., 10, 5360, 10.1038/s41467-019-13355-3 Feng, 2015, K+ accumulation in the cytoplasm and nucleus of the salt gland cells of Limonium bicolor accompanies increased rates of salt secretion under NaCl treatment using NanoSIMS, Plant Sci., 238, 286, 10.1016/j.plantsci.2015.06.021 Feng, 2014, Study on pathway and characteristics of ion secretion of salt glands of Limonium bicolor, Acta Physiologiae Plantarum, 36, 2729, 10.1007/s11738-014-1644-3 Flowers, 2010, Evolution of halophytes: multiple origins of salt tolerance in land plants, Funct. Plant Biol., 37, 604, 10.1071/FP09269 Gao, 2008, SAD2 in Arabidopsis functions in trichome initiation through mediating GL3 function and regulating GL1, TTG1 and GL2 expression, J. Integr. Plant Biol., 50, 906, 10.1111/j.1744-7909.2008.00695.x Hulse-Kemp, 2021, An anchored chromosome-scale genome assembly of spinach improves annotation and reveals extensive gene rearrangements in euasterids, Plant Genome, 14, e20101, 10.1002/tpg2.20101 Hunt, 2020, A chromosome-scale Assembly of the garden orach (Atriplex hortensis L.) genome using oxford nanopore sequencing, Front. Plant Sci., 11, 624, 10.3389/fpls.2020.00624 Ishida, 2007, Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation, Plant Cell, 19, 2531, 10.1105/tpc.107.052274 Jarvis, 2017, The genome of Chenopodium quinoa, Nature, 542, 307, 10.1038/nature21370 Johnson, 2002, TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor, Plant Cell, 14, 1359, 10.1105/tpc.001404 Kang, 2009, The MYB23 gene provides a positive feedback loop for cell fate specification in the Arabidopsis root epidermis, Plant Cell, 21, 1080, 10.1105/tpc.108.063180 Kariyat, 2018, Leaf trichomes affect caterpillar feeding in an instar-specific manner, Commun. Integr. Biol., 11, 1, 10.1080/19420889.2018.1486653 Kim, 2019, Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype, Nat. Biotechnol., 37, 907, 10.1038/s41587-019-0201-4 Kirik, 2004, The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis, Dev. Biol., 268, 506, 10.1016/j.ydbio.2003.12.037 Kirik, 2004, ENHANCER of TRY and CPC 2 (ETC2) reveals redundancy in the region-specific control of trichome development of Arabidopsis, Plant Mol. Biol., 55, 389, 10.1007/s11103-004-0893-8 Kobayashi, 2007, Ability of salt glands in Rhodes grass (Chloris gayana Kunth) to secrete Na+ and K+, Soil Sci. Plant Nutr., 53, 764, 10.1111/j.1747-0765.2007.00192.x Leng, 2019, The lb23 mutant of recretohalophyte Limonium bicolor (Bag.) Kuntze with 20-24-28- and 32-cell salt glands shows elevated salt secretion, Flora, 259, 151441, 10.1016/j.flora.2019.151441 Leng, 2021, Heterologous expression of the Limonium bicolor MYB transcription factor LbTRY in Arabidopsis thaliana increases salt sensitivity by modifying root hair development and osmotic homeostasis, Plant Sci., 302, 110704, 10.1016/j.plantsci.2020.110704 Li, 2021, Subtelomeric assembly of a multi-gene pathway for antimicrobial defense compounds in cereals, Nat. Commun., 12, 2563, 10.1038/s41467-021-22920-8 Lu, 2020, The SNARE protein LbSYP61 participates in salt secretion in Limonium bicolor, Environ. Exp. Bot., 176, 104076, 10.1016/j.envexpbot.2020.104076 Ma, 2021, A chromosome-level Amaranthus cruentus genome assembly highlights gene family evolution and biosynthetic gene clusters that may underpin the nutritional value of this traditional crop, Plant J. : Cel. Mol. Biol., 107, 613, 10.1111/tpj.15298 Ma, 2015, A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants, Mol. Plant, 8, 1274, 10.1016/j.molp.2015.04.007 Mangelson, 2019, The genome of Chenopodium pallidicaule: an emerging Andean super grain, Appl. Plant Sci., 7, e11300, 10.1002/aps3.11300 Meinke, 1994, Seed development in Arabidopsis thaliana, Cold Spring Harbor Monogr. Archive, 27, 253 Montgomery, 2020, Draft genomes of Amaranthus tuberculatus, Amaranthus hybridus, and Amaranthus palmeri, Genome Biol. Evol., 12, 1988, 10.1093/gbe/evaa177 Morohashi, 2007, Participation of the Arabidopsis bHLH factor GL3 in trichome initiation regulatory events, Plant Physiol., 145, 736, 10.1104/pp.107.104521 Munns, 2008, Mechanisms of salinity tolerance, Annu. Rev. Plant Biol., 59, 651, 10.1146/annurev.arplant.59.032607.092911 Murashige, 1962, A revised medium for rapid growth and bio assays with tobacco tissue cultures, Physiol. Plantarum, 15, 473, 10.1111/j.1399-3054.1962.tb08052.x MyeongMin, 1999, WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning, Cell, 99, 473, 10.1016/S0092-8674(00)81536-6 Nadeau, 2002, Stomatal development in Arabidopsis, 1 Neller, 2019, De novo assembly of the pokeweed genome provides insight into pokeweed antiviral protein (PAP) gene expression, Front. Plant Sci., 10, 1002, 10.3389/fpls.2019.01002 Olsen, 2016, The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea, Nature, 530, 331, 10.1038/nature16548 Olsson, 2009, Localization of enzymes of artemisinin biosynthesis to the apical cells of glandular secretory trichomes of Artemisia annua L, Phytochemistry, 70, 1123, 10.1016/j.phytochem.2009.07.009 Oppenheimer, 1991, A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules, Cell, 67, 483, 10.1016/0092-8674(91)90523-2 Palfalvi, 2020, Genomes of the Venus flytrap and close relatives unveil the roots of plant carnivory, Curr. Biol., 30, 2312, 10.1016/j.cub.2020.04.051 Patterson, 2019, The draft genome of Kochia scoparia and the mechanism of glyphosate resistance via transposon-mediated EPSPS tandem gene duplication, Genome Biol. Evol., 11, 2927, 10.1093/gbe/evz198 Payne, 2000, GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1, Genetics, 156, 1349, 10.1093/genetics/156.3.1349 Pesch, 2004, Creating a two-dimensional pattern de novo during Arabidopsis trichome and root hair initiation, Curr. Opin. Genet. Dev., 14, 422, 10.1016/j.gde.2004.06.007 Pesch, 2009, One, two, three, models for trichome patterning in Arabidopsis?, Curr. Opin. Plant Biol., 12, 587, 10.1016/j.pbi.2009.07.015 Pottier, 2020, Identification of two new trichome-specific promoters of Nicotiana tabacum, Planta, 251, 58, 10.1007/s00425-020-03347-9 Qiu, 2002, Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3, Proc. Natl. Acad. Sci. U S A, 99, 8436, 10.1073/pnas.122224699 Ramadan, 2004, Effects of salinity and benzyl adenine on development and function of microhairs of Zea mays L, Planta, 219, 639, 10.1007/s00425-004-1269-7 Ren, 2005, A rice quantitative trait locus for salt tolerance encodes a sodium transporter, Nat. Genet., 37, 1141, 10.1038/ng1643 Rerie, 1994, The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis, Genes Develop., 8, 1388, 10.1101/gad.8.12.1388 Rifkin, 2021, Widespread recombination suppression facilitates plant sex chromosome evolution, Mol. Biol. Evol., 38, 1018, 10.1093/molbev/msaa271 Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 Rodríguez Del Río, 2019, Genomes of the wild beets Beta patula and Beta vulgaris ssp. maritima, Plant J. : Cel. Mol. Biol., 99, 1242, 10.1111/tpj.14413 Rozewicki, 2019, MAFFT-DASH: integrated protein sequence and structural alignment, Nucleic Acids Res., 47, W5 Schnittger, 1999, Generation of a spacing pattern: the role of TRIPTYCHON in trichome patterning in Arabidopsis, Plant Cell, 11, 1105, 10.1105/tpc.11.6.1105 Shabala, 2015, Salt stress sensing and early signalling events in plant roots: current knowledge and hypothesis, Plant Sci., 241, 109, 10.1016/j.plantsci.2015.10.003 Shi, 2000, The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter, Proc. Natl. Acad. Sci. U S A, 97, 6896, 10.1073/pnas.120170197 Shi, 2007, Karyotype Analysis of bicolor statice (Limonium bicolor (Bunge) Kuntze), J. Tianjin Agric. Univ., 36, 7 Shimony, 1968, Light and electron microscopical studies on the structure of salt glands of Tamarix aphylla L, J. Linn. Soc. Lond. Bot., 60, 283, 10.1111/j.1095-8339.1968.tb00090.x Sturtevant, 2020, The genome of jojoba (Simmondsia chinensis): a taxonomically isolated species that directs wax ester accumulation in its seeds, Sci. Adv., 6, eaay3240, 10.1126/sciadv.aay3240 Tominaga, 2008, Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation, Development, 135, 1335, 10.1242/dev.017947 Wada, 1997, Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC, CPC. Sci., 277, 1113 Walker, 1999, The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein, Plant Cell, 11, 1337, 10.1105/tpc.11.7.1337 Wang, 2019, A draft genome assembly of halophyte Suaeda aralocaspica, a plant that performs C4 photosynthesis within individual cells, GigaScience, 8, giz116, 10.1093/gigascience/giz116 Wang, 2015, The rice high-affinity potassium Transporter1;1 is involved in salt tolerance and regulated by an MYB-type transcription factor, Plant Physiol., 168, 1076, 10.1104/pp.15.00298 Wang, 2008, Comprehensive analysis of single-repeat R3 MYB proteins in epidermal cell patterning and their transcriptional regulation in Arabidopsis, BMC Plant Biol., 8, 81, 10.1186/1471-2229-8-81 Wang, 2007, TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis, Development, 134, 3873, 10.1242/dev.009597 Wang, 2021, A novel gene LbHLH from the halophyte Limonium bicolor enhances salt tolerance via reducing root hair development and enhancing osmotic resistance, BMC Plant Biol., 21, 284, 10.1186/s12870-021-03094-3 Wester, 2009, Functional diversity of R3 single-repeat genes in trichome development, Development, 136, 1487, 10.1242/dev.021733 Yagi, 2014, Sequence analysis of the genome of carnation (Dianthus caryophyllus L.), DNA Res., 21, 231, 10.1093/dnares/dst053 Yang, 2013, Trichomes as models for studying plant cell differentiation, Cell Mol. Life Sci., 70, 1937, 10.1007/s00018-012-1147-6 Yang, 2018, Improved transcriptome sampling pinpoints 26 ancient and more recent polyploidy events in Caryophyllales, including two allopolyploidy events, New Phytol., 217, 855, 10.1111/nph.14812 Yang, 2019, The Ca2+ sensor SCaBP3/CBL7 modulates plasma membrane H+-ATPase activity and promotes alkali tolerance in Arabidopsis, Plant Cell, 31, 1367, 10.1105/tpc.18.00568 Yasui, 2016, Assembly of the draft genome of buckwheat and its applications in identifying agronomically useful genes, DNA Res., 23, 215, 10.1093/dnares/dsw012 Yuan, 2013, An efficient autofluorescence method for screening Limonium bicolor mutants for abnormal salt gland density and salt secretion, South Afr. J. Bot., 88, 110, 10.1016/j.sajb.2013.06.007 Yuan, 2014, A system for the transformation and regeneration of the recretohalophyte Limonium bicolor, In Vitro Cell Develop. Biol. Plant, 50, 610, 10.1007/s11627-014-9611-7 Yuan, 2014, The observation of pollen viability and pollen tube germination in Limonium bicolor, WIT Trans. Biomed. Health, 18, 631, 10.2495/HHME130841 Yuan, 2019, Reproductive physiology of halophytes: current standing, Front. Plant Sci., 9, 1954, 10.3389/fpls.2018.01954 Yuan, 2019, A WD40-repeat protein from the recretohalophyte Limonium bicolor enhances trichome formation and salt tolerance in Arabidopsis, Front. Plant Sci., 10, 1456, 10.3389/fpls.2019.01456 Yuan, 2016, Progress in studying salt secretion from the salt glands in recretohalophytes: how do plants secrete salt?, Front. Plant Sci., 7, 977, 10.3389/fpls.2016.00977 Yuan, 2019, Methyl jasmonate improves salinity tolerance in Limonium bicolor by enhancing photosynthesis and abaxial salt gland density, Funct. Plant Biol. Online, 46, 82, 10.1071/FP18120 Yuan, 2016, The transcriptome of NaCl-treated Limonium bicolor leaves reveals the genes controlling salt secretion of salt gland, Plant Mol. Biol., 91, 241, 10.1007/s11103-016-0460-0 Yuan, 2015, Comparative transcriptome analysis of developmental stages of the Limonium bicolor leaf generates insights into salt gland differentiation, Plant Cell Environ., 38, 1637, 10.1111/pce.12514 Yuan, 2020, Adaptation of Recretohalophytes to Salinity, 1 Zhang, 2011, The development and geometry of shape change in Arabidopsis thaliana cotyledon pavement cells, BMC Plant Biol., 11, 27, 10.1186/1471-2229-11-27 Zhang, 2003, A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis, Development, 130, 4859, 10.1242/dev.00681 Zhang, 2017, The tartary buckwheat genome provides insights into rutin biosynthesis and abiotic stress tolerance, Mol. Plant, 10, 1224, 10.1016/j.molp.2017.08.013 Zhang, 2018, A retrotransposon in an HKT1 family sodium transporter causes variation of leaf Na+ exclusion and salt tolerance in maize, New Phytol., 217, 1161, 10.1111/nph.14882 Zhang, 2009, IRREGULAR TRICHOME BRANCH 2 (ITB2) encodes a putative aminophospholipid translocase that regulates trichome branch elongation in Arabidopsis, Plant J., 60, 195, 10.1111/j.1365-313X.2009.03954.x Zhang, 2019, Assembly and annotation of a draft genome of the medicinal plant polygonum cuspidatum, Front. Plant Sci., 10, 1274, 10.3389/fpls.2019.01274 Zhao, 2008, The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci, Development, 135, 1991, 10.1242/dev.016873 Zhao, 2008, The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci, Development, 135, 1991, 10.1242/dev.016873 Zheng, 2021, The chromosome-level genome of dragon fruit reveals whole-genome duplication and chromosomal co-localization of betacyanin biosynthetic genes, Hortic. Res., 8, 63, 10.1038/s41438-021-00501-6 Zhou, 2014, Inhibition of the Arabidopsis salt overly sensitive pathway by 14-3-3 proteins, Plant Cell, 26, 1166, 10.1105/tpc.113.117069 Zhou, 2018, Effects of salt stress on plant growth, antioxidant capacity, glandular trichome density, and volatile exudates of Schizonepeta tenuifolia Briq, Int. J. Mol. Sci., 19, 252, 10.3390/ijms19010252 Zhu, 2016, Abiotic stress signaling and responses in plants, Cell, 167, 313, 10.1016/j.cell.2016.08.029 Ziegler, 1967, Die Salzdrüsen von Limonium vulgare, Planta, 74, 1, 10.1007/BF00385168 Zou, 2019, The genome of broomcorn millet, Nat. Commun., 10, 436, 10.1038/s41467-019-08409-5