Transcriptional changes during crown-root development and emergence in barley (Hordeum vulgare L.)
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články
PubMed
38778283
PubMed Central
PMC11110440
DOI
10.1186/s12870-024-05160-y
PII: 10.1186/s12870-024-05160-y
Knihovny.cz E-zdroje
- Klíčová slova
- Barley (Hordeum vulgare L.), Crown roots, Emergence, Transcriptome,
- MeSH
- ječmen (rod) * genetika růst a vývoj metabolismus MeSH
- kořeny rostlin * růst a vývoj genetika metabolismus MeSH
- regulace genové exprese u rostlin * MeSH
- rostlinné geny MeSH
- semenáček růst a vývoj genetika MeSH
- stanovení celkové genové exprese MeSH
- transkriptom MeSH
- Publikační typ
- časopisecké články MeSH
BACKGROUND: Roots play an important role during plant growth and development, ensuring water and nutrient uptake. Understanding the mechanisms regulating their initiation and development opens doors towards root system architecture engineering. RESULTS: Here, we investigated by RNA-seq analysis the changes in gene expression in the barley stem base of 1 day-after-germination (DAG) and 10DAG seedlings when crown roots are formed. We identified 2,333 genes whose expression was lower in the stem base of 10DAG seedlings compared to 1DAG seedlings. Those genes were mostly related to basal cellular activity such as cell cycle organization, protein biosynthesis, chromatin organization, cytoskeleton organization or nucleotide metabolism. In opposite, 2,932 genes showed up-regulation in the stem base of 10DAG seedlings compared to 1DAG seedlings, and their function was related to phytohormone action, solute transport, redox homeostasis, protein modification, secondary metabolism. Our results highlighted genes that are likely involved in the different steps of crown root formation from initiation to primordia differentiation and emergence, and revealed the activation of different hormonal pathways during this process. CONCLUSIONS: This whole transcriptomic study is the first study aiming at understanding the molecular mechanisms controlling crown root development in barley. The results shed light on crown root emergence that is likely associated with a strong cell wall modification, death of the cells covering the crown root primordium, and the production of defense molecules that might prevent pathogen infection at the site of root emergence.
Czech Advanced Technology and Research Institute Palacký University Olomouc Olomouc Czechia
Department of Biochemistry Faculty of Science Palacký University Olomouc Olomouc Czechia
Present address Masaryk Memorial Cancer Institute Brno Czechia
UMR DIADE Université de Montpellier IRD CIRAD Montpellier France
Zobrazit více v PubMed
Gonin, Bergougnoux, Nguyen, Gantet, Champion What makes adventitious roots? Plants. 2019;8:240. doi: 10.3390/plants8070240. PubMed DOI PMC
López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L. The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol. 2003;6:280–287. doi: 10.1016/S1369-5266(03)00035-9. PubMed DOI
Gao Y, Lynch JP. Reduced crown root number improves water acquisition under water deficit stress in maize (Zea mays L.) J Ex Bot. 2016;67:4545–57. doi: 10.1093/jxb/erw243. PubMed DOI PMC
Li X, Zeng R, Liao H. Improving crop nutrient efficiency through root architecture modifications. J Integr Plant Biol. 2016;58:193–202. doi: 10.1111/jipb.12434. PubMed DOI
Li A, Zhu L, Xu W, Liu L, Teng G. Recent advances in methods for in situ root phenotyping. PeerJ. 2022;10:e13638. doi: 10.7717/peerj.13638. PubMed DOI PMC
Ciais P, Reichstein M, Viovy N, Granier A, Ogée J, Allard V, et al. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature. 2005;437(7058):529–533. doi: 10.1038/nature03972. PubMed DOI
Ray DK, Gerber JS, Macdonald GK, West PC. Climate variation explains a third of global crop yield variability. Nat Commun. 2015;6(1):5989. doi: 10.1038/ncomms6989. PubMed DOI PMC
Bellini C, Pacurar DI, Perrone I. Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol. 2014;65:639–666. doi: 10.1146/annurev-arplant-050213-035645. PubMed DOI
Smith S, De Smet I. Root system architecture: insights from arabidopsis and cereal crops. Philos Trans R Soc B Biol Sci. 2012;367:1441–1452. doi: 10.1098/rstb.2011.0234. PubMed DOI PMC
Atkinson JA, Rasmussen A, Traini R, Voss U, Sturrock C, Mooney SJ, et al. Branching Out in Roots: uncovering form, function and regulation. Plant Physiol. 2014;166:538–550. doi: 10.1104/pp.114.245423. PubMed DOI PMC
Lo S-F, Fan M-J, Hsing Y-I, Chen L-J, Chen S, Wen I-C, et al. Genetic resources offer efficient tools for rice functional genomics research. Plant Cell Environ. 2016;39(5):998–1013. doi: 10.1111/pce.12632. PubMed DOI
Mai CD, Phung NT, To HT, Gonin M, Hoang GT, Nguyen KL, et al. Genes controlling root development in rice. Rice (N Y) 2014;7(1):30. doi: 10.1186/s12284-014-0030-5. PubMed DOI PMC
Meng F, Xiang D, Zhu J, Li Y, Mao C. Molecular mechanisms of root development in rice. Rice. 2019;12(1):1. doi: 10.1186/s12284-018-0262-x. PubMed DOI PMC
Pasam RK, Sharma R, Walther A, Özkan H, Graner A, Kilian B. Genetic diversity and population structure in a legacy collection of spring barley landraces adapted to a wide range of climates. PLoS One. 2014;9:1–29. doi: 10.1371/journal.pone.0116164. PubMed DOI PMC
Milner SG, Jost M, Taketa S, Mazón ER, Himmelbach A, Oppermann M, et al. Genebank genomics highlights the diversity of a global barley collection. Nat Genet. 2019;51:319–326. doi: 10.1038/s41588-018-0266-x. PubMed DOI
Mayer KFX, Martis M, Hedley PE, Simková H, Liu H, Morris JA, et al. Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell. 2011;23:1249–1263. doi: 10.1105/tpc.110.082537. PubMed DOI PMC
Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, et al. A chromosome conformation capture ordered sequence of the barley genome. Nature. 2017;544:427–433. doi: 10.1038/nature22043. PubMed DOI
Mascher M, Wicker T, Jenkins J, Plott C, Lux T, Koh CS, et al. Long-read sequence assembly: a technical evaluation in barley. Plant Cell. 2021;33(6):1888–1906. doi: 10.1093/plcell/koab077. PubMed DOI PMC
Monat C, Padmarasu S, Lux T, Wicker T, Gundlach H, Himmelbach A, et al. TRITEX: chromosome-scale sequence assembly of Triticeae genomes with open-source tools. Genome Biol. 2019;20:284. doi: 10.1186/s13059-019-1899-5. PubMed DOI PMC
Marthe C, Kumlehn J, Hensel G. Barley (Hordeum vulgare L.) transformation using immature embryos. In: Wang K, editor. Agrobacterium Protocols: Volume 1. Springer, New York: New York, NY; 2015. pp. 71–83. PubMed
Kumlehn J, Serazetdinova L, Hensel G, Becker D, Loerz H. Genetic transformation of barley (Hordeum vulgare L.) via infection of androgenetic pollen cultures with Agrobacterium tumefaciens. Plant Biotechnol J. 2006;4:251–61. doi: 10.1111/j.1467-7652.2005.00178.x. PubMed DOI
Vlamis J, Williams DE. Ion competition in Manganese uptake by barley plants. Plant Physiol. 1962;37:650–655. doi: 10.1104/pp.37.5.650. PubMed DOI PMC
Lavarenne J, Gonin M, Guyomarc'h S, Rouster J, Champion A, Sallaud C, et al. Inference of the gene regulatory network acting downstream of CROWN ROOTLESS 1 in rice reveals a regulatory cascade linking genes involved in auxin signaling, crown root initiation, and root meristem specification and maintenance. Plant J. 2019;100:954–968. doi: 10.1111/tpj.14487. PubMed DOI
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676–682. doi: 10.1038/nmeth.2019. PubMed DOI PMC
Mergemann H, Sauter M. Ethylene induces epidermal cell death at the site of adventitious root emergence in rice. Plant Physiol. 2000;124:609–614. doi: 10.1104/pp.124.2.609. PubMed DOI PMC
International Barley Genome Sequencing C A physical, genetic and functional sequence assembly of the barley genome. Nature. 2012;491(7426):711–6. doi: 10.1038/nature11543. PubMed DOI
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;14(4):R36. doi: 10.1186/gb-2013-14-4-r36. PubMed DOI PMC
Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2014;31(2):166–169. doi: 10.1093/bioinformatics/btu638. PubMed DOI PMC
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550. doi: 10.1186/s13059-014-0550-8. PubMed DOI PMC
Lohse M, Nagel A, Herter T, May P, Schroda M, Zrenner R, et al. Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data. Plant Cell Environ. 2014;37:1250–1258. doi: 10.1111/pce.12231. PubMed DOI
Schwacke R, Ponce-Soto GY, Krause K, Bolger AM, Arsova B, Hallab A, et al. MapMan4: a refined protein classification and annotation framework applicable to multi-omics data analysis. Mol Plant. 2019;12:879–892. doi: 10.1016/j.molp.2019.01.003. PubMed DOI
Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, et al. Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 2004;37(6):914–939. doi: 10.1111/j.1365-313X.2004.02016.x. PubMed DOI
Klie S, Nikoloski Z. The choice between MapMan and gene ontology for automated gene function prediction in plant science. Front Genet. 2012;3:115. doi: 10.3389/fgene.2012.00115. PubMed DOI PMC
Ge SX, Jung D, Yao R. ShinyGO: a graphical gene-set enrichment tool for animals and plants. Bioinformatics. 2020;36(8):2628–2629. doi: 10.1093/bioinformatics/btz931. PubMed DOI PMC
Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, et al. Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinform. 2008;2008:1–5. doi: 10.1155/2008/420747. PubMed DOI PMC
Xie F, Xiao P, Chen D, Xu L, Zhang B. miRDeepFinder: a miRNA analysis tool for deep sequencing of plant small RNAs. Plant Mol Biol. 2012;80(1):75–84. doi: 10.1007/s11103-012-9885-2. PubMed DOI
Hua W, Zhu J, Shang Y, Wang J, Jia Q, Yang J. Identification of suitable reference genes for barley gene expression under abiotic stresses and hormonal treatments. Plant Mol Biol Rep. 2015;33(4):1002–1012. doi: 10.1007/s11105-014-0807-0. DOI
Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45. doi: 10.1093/nar/29.9.e45. PubMed DOI PMC
Chow C-N, Lee T-Y, Hung Y-C, Li G-Z, Tseng K-C, Liu Y-H, et al. PlantPAN3.0: a new and updated resource for reconstructing transcriptional regulatory networks from ChIP-seq experiments in plants. Nucleic Acids Res. 2019;47:D1155–D63. doi: 10.1093/nar/gky1081. PubMed DOI PMC
Coudert Y, Périn C, Courtois B, Khong NG, Gantet P. Genetic control of root development in rice, the model cereal. Trends Plant Sci. 2010;15:219–226. doi: 10.1016/j.tplants.2010.01.008. PubMed DOI
Coudert Y, Le VAT, Gantet P. Rice: a model plant to decipher the hidden origin of adventitious roots. Plant roots, the hidden half. 2013.
Itoh JI, Nonomura KI, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, et al. Rice plant development: From zygote to spikelet. Plant Cell Physiol. 2005;46:23–47. doi: 10.1093/pcp/pci501. PubMed DOI
Xu J, Hong JH. Root Development. In: Zhang Q, Wing R, editors. Genetics and Genomics of Rice. Plant Genetics and Genomics: Crops and Models, vol 5. New York: Springer; 2013. 10.1007/978-1-4614-7903-1_20.
Hochholdinger F, Woll K, Sauer M, Dembinsky D. Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes. Ann Bot. 2004;93(4):359–368. doi: 10.1093/aob/mch056. PubMed DOI PMC
Li J, Xu Y, Chong K. The novel functions of kinesin motor proteins in plants. Protoplasma. 2012;249:95–100. doi: 10.1007/s00709-011-0357-3. PubMed DOI PMC
Himanen K, Boucheron E, Vanneste S, de Almeida EJ, Inzé D, Beeckman T. Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell. 2002;14(10):2339–2351. doi: 10.1105/tpc.004960. PubMed DOI PMC
Fukaki H, Okushima Y, Tasaka M. Auxin-mediated lateral root formation in higher plants. Int Rev Cytol.2007;256:111-37. 10.1016/S0074-7696(07)56004-3. PubMed
Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN. Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science. 2010;329:1306–1311. doi: 10.1126/science.1191937. PubMed DOI PMC
Kitomi Y, Ogawa A, Kitano H, Inukai Y. CRL4 regulates crown root formation through auxin transport in rice. Plant Root. 2008;2:19–28. doi: 10.3117/plantroot.2.19. DOI
Liu S, Wang J, Wang L, Wang X, Xue Y, Wu P, et al. Adventitious root formation in rice requires OsGNOM1 and is mediated by the OsPINs family. Cell Res. 2009;19:1110–1119. doi: 10.1038/cr.2009.70. PubMed DOI
LeClere S, Tellez R, Rampey RA, Matsuda SPT, Bartel B. Characterization of a family of IAA-amino acid conjugate hydrolases from Arabidopsis. J Biol Chem. 2002;277:20446–20452. doi: 10.1074/jbc.M111955200. PubMed DOI
Rampey RA, LeClere S, Kowalczyk M, Ljung K, Sandberg G, Bartel B. A family of auxin-conjugate hydrolases that contributes to free indole-3-acetic acid levels during Arabidopsis germination. Plant Physiol. 2004;135(2)978–88. 10.1104/pp.104.039677. PubMed PMC
Humplík JF, Bergougnoux V, Van Volkenburgh E. To stimulate or inhibit? That is the question for the function of abscisic acid. Trends Plant Sci. 2017;xx:1–12. PubMed
Harris J. Abscisic acid: hidden architect of root system structure. Plants. 2015;4:548–572. doi: 10.3390/plants4030548. PubMed DOI PMC
Gou J, Strauss SH, Tsai CJ, Fang K, Chen Y, Jiang X, et al. Gibberellins regulate lateral root formation in populus through interactions with auxin and other hormones. Plant Cell. 2010;22:623–639. doi: 10.1105/tpc.109.073239. PubMed DOI PMC
Lo SF, Yang SY, Chen KT, Hsing YI, Zeevaart JAD, Chen LJ, et al. A novel class of gibberellin 2-oxidases control semidwarfism, tillering, and root development in rice. Plant Cell. 2008;20:2603–2618. doi: 10.1105/tpc.108.060913. PubMed DOI PMC
Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, et al. Slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell. 2001;13:999–1010. doi: 10.1105/tpc.13.5.999. PubMed DOI PMC
Charlton W. Lateral root initiation. In: Waisel Y, Eshel A, Kfkaki U, editors. Plant roots, the hidden half. 2. Marcel Dekker: New York; 1996. pp. 149–73.
Park WJ, Hochholdinger F, Gierl A. Release of the benzoxazinoids defense molecules during lateral- and crown root emergence in Zea mays. J Plant Physiol. 2004;161:981–985. doi: 10.1016/j.jplph.2004.01.005. PubMed DOI
Steffens B, Kovalev A, Gorb SN, Sauter M. Emerging roots alter epidermal cell fate through mechanical and reactive oxygen species signaling. Plant Cell. 2012;24:3296–3306. doi: 10.1105/tpc.112.101790. PubMed DOI PMC
Steffens B, Sauter M. Epidermal cell death in rice is confined to cells with a distinct molecular identity and is mediated by ethylene and H2O2 through an autoamplified signal pathway. Plant Cell. 2009;21:184–196. doi: 10.1105/tpc.108.061887. PubMed DOI PMC
Passarinho PA, de Vries SC. Arabidopsis Chitinases : a genomic survey. Arabidopsis Book. 2002;1:e0023. doi: 10.1199/tab.0023. PubMed DOI PMC
Kim DS, Kim NH, Hwang BK. The Capsicum annuum class IV chitinase ChitIV interacts with receptor-like cytoplasmic protein kinase PIK1 to accelerate PIK1-triggered cell death and defence responses. J Exp Bot. 2015;66:1987–1999. doi: 10.1093/jxb/erv001. PubMed DOI PMC
Péret B, De Rybel B, Casimiro I, Benková E, Swarup R, Laplaze L, Beeckman T, Bennett MJ. Arabidopsis lateral root development: an emerging story. Trends Plant Sci. 2009;14(7):399-408. 10.1016/j.tplants.2009.05.002. PubMed
Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y, et al. The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol. 2008;10:946–954. doi: 10.1038/ncb1754. PubMed DOI
Roycewicz PS, Malamy JE. Cell wall properties play an important role in the emergence of lateral root primordia from the parent root. J Exp Bot. 2014;65:2057–2069. doi: 10.1093/jxb/eru056. PubMed DOI PMC
Makowska B, Bakera B, Rakoczy-Trojanowska M. The genetic background of benzoxazinoid biosynthesis in cereals. Acta Physiol Plant. 2015;37:1–12. doi: 10.1007/s11738-015-1927-3. DOI