Systematic analysis of the pectin methylesterase gene family in Nicotiana tabacum and reveal their multiple roles in plant development and abiotic stresses.
Sun, Jinhao; Tian, Zhen; Li, Xiaoxuet al.
2022 • In Frontiers in Plant Science, 13, p. 998841
[en] The pectin methylesterases (PMEs) play multiple roles in regulating plant development and responses to various stresses. In our study, a total of 121 PME genes were identified in the tobacco genome, which were clustered into two groups based on phylogenetic analysis together with Arabidopsis members. The investigations of gene structure and conserved motif indicated that exon/intron and motif organizations were relatively conserved in each group. Additionally, several stress-related elements were identified in the promoter region of these genes. The survey of duplication events revealed that segmental duplications were critical to the expansion of the PME gene family in tobacco. The expression profiles analysis revealed that these genes were expressed in various tissues and could be induced by diverse abiotic stresses. Notably, NtPME029 and NtPME043, were identified as homologues with AtPME3 and AtPME31, respectively. Furthermore, NtPME029 was highly expressed in roots and the over-expression of the NtPME029 gene could promote the development of roots. While NtPME043 could be induced by salt and ABA treatments, and the over-expression of the NtPME043 gene could significantly enhance the salt-stress tolerance in tobacco. Overall, these findings may shed light on the biological and functional characterization of NtPME genes in tobacco.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Sun, Jinhao ✱; Technology Center, China Tobacco Jiangsu Industrial Co., Ltd., Nanjing, China ; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China
Tian, Zhen ✱; Technology Center, China Tobacco Jiangsu Industrial Co., Ltd., Nanjing, China
Li, Xiaoxu ✱; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China
Li, Shaopeng; Technology Center, China Tobacco Jiangsu Industrial Co., Ltd., Nanjing, China
Li, Zhiyuan; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China
Wang, Jinling; Technology Center, China Tobacco Jiangsu Industrial Co., Ltd., Nanjing, China
Hu, Zongyu; Technology Center, China Tobacco Jiangsu Industrial Co., Ltd., Nanjing, China
Chen, Haiqing; Technology Center, China Tobacco Jiangsu Industrial Co., Ltd., Nanjing, China
Guo, Cun; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China ; Kunming Branch of Yunnan Provincial Tobacco Company, Kunming, China
Xie, Minmin ✱; Université de Liège - ULiège > TERRA Research Centre ; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China
Xu, Ruyan ✱; Technology Center, China Tobacco Jiangsu Industrial Co., Ltd., Nanjing, China
✱ These authors have contributed equally to this work.
Language :
English
Title :
Systematic analysis of the pectin methylesterase gene family in Nicotiana tabacum and reveal their multiple roles in plant development and abiotic stresses.
This work was supported by the Optimization of Quality Assurance Technology for China Tobacco special aroma 301 Variety and Its Application in Middle and High-end Cigarettes (Y02J202102); the Agricultural Science and Technology Innovation Program (ASTIP-TRIC02); the China Tobacco Genome Project [110202001029(JY-12)] and the China Tobacco Hunan Industrial Co., Ltd. Technology Project (KY2022YC0010).
Al-Qsous S. Carpentier E. Klein-Eude D. Burel C. Mareck A. Dauchel H. et al. (2004). Identification and isolation of a pectin methylesterase isoform that could be involved in flax cell wall stiffening. Planta. 219, 369–378. doi: 10.1007/s00425-004-1246-1
An S. H. Sohn K. H. Choi H. W. Hwang I. S. Lee S. C. Hwang B. K. (2008). Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance, and abiotic stress tolerance. Planta. 228, 61–78. doi: 10.1007/s00425-008-0719-z
Bailey T. L. Johnson J. Grant C. E. Noble W. S. (2015). The MEME suite. Nucleic Acids Res. 43, W39–W49. doi: 10.1093/nar/gkv416
Bosch M. Cheung A. Y. Hepler P. K. (2005). Pectin methylesterase, a regulator of pollen tube growth. Plant Physiol. 138, 1334–1346. doi: 10.1104/pp.105.059865
Buschmann H. (2016). Plant cell division analyzed by transient agrobacterium-mediated transformation of tobacco BY-2 cells. Methods Mol. Biol. 1370, 17–25. doi: 10.1007/978-1-4939-3142-2_2
Cao Y. Han Y. Li D. Lin Y. Cai Y. (2016). MYB transcription factors in Chinese pear (Pyrus bretschneideri rehd.): Genome-wide identification, classification, and expression profiling during fruit development. Front. Plant Sci. 7. doi: 10.3389/fpls.2016.00577
Chen C. J. Chen H. Zhang Y. Thomas H. R. Frank M. H. He Y. H. et al. (2020). TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 13, 1194–1202. doi: 10.1016/j.molp.2020.06.009
Chao J. Kong Y. Wang Q. Sun Y. Liu G. (2015). MapGene2Chrom, a tool to draw gene physical map based on Perl and SVG languages. Hereditas 37, 91–97. doi: 10.16288/j.yczz.2015.01.013
Dixit S. Upadhyay S. K. Singh H. Sidhu O. P. Verma P. C. Chandrashekar C. (2013). Enhanced methanol production in plants provides broad spectrum insect resistance. PloS One 8, e79664. doi: 10.1371/journal.pone.0079664
Duan W. Huang Z. Song X. Liu T. Liu H. Hou X. et al. (2016). Comprehensive analysis of the polygalacturonase and pectin methylesterase genes in Brassica rapa shed light on their different evolutionary patterns. Sci. Rep. 6, 25107. doi: 10.1038/srep25107
Edwards K. D. Fernandez-Pozo N. Drake-Stowe K. Humphry M. Evans A. D. Bombarely A. et al. (2017). A reference genome for Nicotiana tabacum enables map-based cloning of homeologous loci implicated in nitrogen efficiency. BMC Genom. 18, 448. doi: 10.1186/s12864-017-3791-6
Finn R. D. Coggill P. Eberhardt R. Y. Eddy S. R. Mistry J. Mitchell A. L. et al. (2016). The pfam protein families database: Towards a more sustainable future. Nucleic Acids Res. 44, D279–D285. doi: 10.1093/nar/gkv1344
Garg V. K. Avashthi H. Tiwari A. (2016). MFPPI–multi FASTA protparam interface. Bioinformation. 12, 74–77. doi: 10.6026/97320630012074
Hewezi T. Howe P. Maier T.,. R. Hussey R. S. Mitchum M. G. Davis E. L. et al. (2008). Cellulose binding protein from the parasitic nematode heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell. 20, 3080–3093. doi: 10.1105/tpc.108.063065
Hongo S. Sato K. Yokoyama R. Nishitani K. (2012). Demethylesterification of the primary wall by PECTIN METHYLESTERASE35 provides mechanical support to the Arabidopsis stem. Plant Cell. 24, 2624–2634. doi: 10.1105/tpc.112.099325
Huang Y. C. Wu H. C. Wang Y. D. Liu C. H. Lin C. C. Luo D. L. et al. (2017). PECTIN METHYLESTERASE34 contributes to heat tolerance through its role in promoting stomatal movement. Plant Physiol. 174, 748–763. doi: 10.1104/pp.17.00335
Hu B. Jin J. P. Guo A. Y. Zhang H. Luo J. C. Gao G. (2015). GSDS 2.0: An upgraded gene feature visualization server. Bioinf. 31(8), 1296–1297. doi: 10.1093/bioinformatics/btu817
Jenkins J. Mayans O. Smith D. Worboys K. Pickersgill R. W. (2001). The third-dimensional structure of erwinia chrysanthemi pectin methylesterase reveals a novel esterase active site. J. Mol. Biol. 305, 951–960. doi: 10.1006/jmbi.2000.4324
Jeong H. Y. Nguyen H. P. Lee C. (2015). Genome-wide identification and expression analysis of rice pectin methylesterases: Implication of functional roles of pectin modification in rice physiology. J. Plant Physiol. 183, 23. doi: 10.1016/j.jplph.2015.05.001
Jiangtao C. Yingzhen K. Qian W. Yuhe S. Guanshan L. (2015). MapGene2Chrom, a tool to draw gene physical map based on Perl and SVG languages. Hereditas. 37, 91. doi: 10.16288/j.yczz.2015.01.013
Khan N. Fatima F. Haider M. S. Shazadee H. Liu Z. Zheng T. et al. (2019). Genome-wide identification and expression profiling of the polygalacturonase (PG) and pectin methylesterase (PME) genes in grapevine (Vitisvinifera l.). Int. J. Mol. Sci. 20 (13), 3180. doi: 10.3390/ijms20133180
Kumar S. Stecher G. Li M. Knyaz C. Tamura K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549. doi: 10.1093/molbev/msy096
Larkin M. A. Blackshields G. Brown N. P. Chenna R. McGettigan P. A. McWilliam H. et al. (2007). Clustal W and clustal X version 2.0. Bioinformatics. 23, 2947–2948. doi: 10.1093/bioinformatics/btm404
Leroux C. Bouton S. Kiefer-Meyer M. C. Fabrice T. N. Mareck A. Guénin S. et al. (2015). PECTIN METHYLESTERASE48 is involved in Arabidopsis pollen grain germination. Plant Physiol. 167, 367–380. doi: 10.1104/pp.114.250928
Lescot M. Dehais P. Thijs G. Marchal K. Moreau Y. Van de Peer Y. et al. (2002). PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30, 325–327. doi: 10.1093/nar/30.1.325
Letunic I. Doerks T. Bork P. (2015). SMART: Recent updates, new developments and status in 2015. Nucleic Acids Res. 43, D257–D260. doi: 10.1093/nar/gku949
Levesque-Tremblay G. Müller K. Mansfield S. D. Haughn G. W. (2015). Highly methyl esterified seeds is a pectin methyl esterase involved in embryo development. Plant Physiol. 167, 725–737. doi: 10.1104/pp.114.255604
Li X. Hamyat M. Liu C. Ahmad S. Gao X. Guo C. et al. (2018). Identification and characterization of the WOX family genes in five solanaceae species reveal their conserved roles in peptide signaling. Genes. 9, 260. doi: 10.3390/genes9050260
Li X. Ahmad S. Ali A. Guo C. Li H. Yu J. et al. (2019a). Characterization of somatic embryogenesis receptor-like kinase 4 as a negative regulator of leaf senescence in Arabidopsis. Cells. 8, 50. doi: 10.3390/cells8010050
Li X. Guo C. Ahmad S. Wang Q. Yu J. Liu C. et al. (2019b). Systematic analysis of MYB family genes in potato and their multiple roles in development and stress responses. Biomolecules. 9 (8), 317. doi: 10.3390/biom9080317
Li Y. He H. He L.,. F. (2020). Genome-wide analysis of the pectin methylesterase gene family in potato. Potato Res. 64, 1–19. doi: 10.1007/s11540-020-09453-1
Li Z. Chao J. Li X. Li G. Song D. Guo Y. et al. (2021). Systematic analysis of the bZIP family in tobacco and functional characterization of NtbZIP62 involvement in salt stress. Agronomy. 11, 148. doi: 10.3390/agronomy11010148
Librado P. Rozas J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 25, 1451–1452. doi: 10.1093/bioinformatics/btp187
Livak K. J. Schmittgen T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-delta delta c (T)) method. Methods. 25, 402–408. doi: 10.1006/meth.2001.1262
Louvet R. Cavel E. Gutierrez L. Guénin S. Roger D. Gillet F. et al. (2006). Comprehensive expression profiling of the pectin methylesterase gene family during silique development in Arabidopsis thaliana. Planta. 224 (4), 782–791. doi: 10.1007/s00425-006-0261-9
Markovic O. Janecek S. (2004). Pectin methylesterases: sequence-structural features and phylogenetic relationships. Carbohydr Res. 339 (13), 2281–2295. doi: 10.1016/j.carres.2004.06.023
Micheli F. (2001). Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Science. 6, 414–419. doi: 10.1016/s1360-1385(01)02045-3
Peaucelle A. Braybrook S. A. Le Guillou L. Bron E. Kuhlemeier C. Höfte H. (2011). Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr. Biol. 21, 1720–1726. doi: 10.1016/j.cub.2011.08.057
Pelloux J. Rustérucci C. Mellerowicz E. J. (2007). New insights into pectin methylesterase structure and function. Trends Plant Sci. 12 (6), 267–277. doi: 10.1016/j.tplants.2007.04.001
Qu T. Liu R. Wang W. An L. Chen T. Liu G. et al. (2011). Brassinosteroids regulate pectin methylesterase activity and AtPME41 expression in Arabidopsis under chilling stress. Cryobiology. 63, 111–117. doi: 10.1016/j.cryobiol.2011.07.003
Ren A. Ahmed R. I. Chen H. Han L. Sun J. Ding A. et al. (2019). Genome-wide identification, characterization and expression patterns of the pectin methylesterase inhibitor genes in sorghum bicolor. Genes. 10 (10), 755. doi: 10.3390/genes10100755
Sénéchal F. Graff L. Surcouf O. Marcelo P. Rayon C. Bouton S. et al. (2014). Arabidopsis PECTIN METHYLESTERASE17 is co-expressed with and processed by SBT3.5, a subtilisin-like serine protease. Ann. Bot. 114, 1161–1175. doi: 10.1093/aob/mcu035
Sun J. Xie M. Li X. Li Z. Sun Y. (2021). Systematic investigations of the ZF-HD gene family in tobacco reveal their multiple roles in abiotic stresses. Agronomy. 11, 406. doi: 10.3390/agronomy11030406
Tian G. W. Chen M. H. Zaltsman A. Citovsky V. (2006). Pollen-specific pectin methylesterase involved in pollen tube growth. Dev. Biol. 294, 83–91. doi: 10.1016/j.ydbio.2006.02.026
Turbant A. Fournet F. Lequart M. Zabijak L. Pageau K. Bouton S. et al. (2016). PME58 plays a role in pectin distribution during seed coat mucilage extrusion through homogalacturonan modification. J. Exp. Bot. 67, 2177–2190. doi: 10.1093/jxb/erw025
Udall J. A. Swanson J. M. Haller K. Rapp R. A. Sparks M. E. Hatfield J. et al. (2006). A global assembly of cotton ESTs. Genome Res. 16, 441–450. doi: 10.1101/gr.4602906
Verma C. Singh R. K. Mishra S. (2014). Biochemical characterization of pectin methylesterase from musa acuminata referring to delayed ripening. IOSR-JPBS. 9, 42–47. doi: 10.9790/3008-49709134247
Wallace S. Williams J. H. (2017). Evolutionary origins of pectin methylesterase genes associated with novel aspects of angiosperm pollen tube walls. Biochem. Biophys. Res. Commun. 487, 509–516. doi: 10.1016/j.bbrc.2017.04.027
Wolf S. Mouille G. Pelloux J. (2009). Homogalacturonan methyl-esterification and plant development. Mol. Plant 2, 851–860. doi: 10.1093/mp/ssp066
Wu X. Lai Y. Lv L. Ji M. Han K. Yan D. et al. (2020). Fasciclin-like arabinogalactan gene family in Nicotiana benthamiana: genome-wide identification, classification and expression in response to pathogens. BMC Plant Biol. 20, 305. doi: 10.1186/s12870-020-02501-5
Xie T. Chen C. Li C. Liu J. Liu C. He Y. (2018). Genome-wide investigation of WRKY gene family in pineapple: Evolution and expression profiles during development and stress. BMC Genom. 19, 490. doi: 10.1186/s12864-018-4880-x
Yan J. He H. Fang L. Zhang A. (2018). Pectin methylesterase31 positively regulates salt stress tolerance in. Arabidopsis. Biochem. Biophys. Res. Commun. 496, 497–501. doi: 10.1016/j.bbrc.2018.01.025
Yapo B. M. Lerouge P. Thibault J. F. Ralet M. C. (2007). Pectins from citrus peel cell walls contain homogalacturonans homogenous with respect to molar mass, rhamnogalacturonan I and rhamnogalacturonan II. Carbohydr. Polym. 69, 426–435. doi: 10.1016/j.carbpol.2006.12.024
Zega A. D'Ovidio R. (2016). Genome-wide characterization of pectin methyl esterase genes reveals members differentially expressed in tolerant and susceptible wheats in response to Fusarium graminearum. Plant Physiol. Biochem. 108, 1–11. doi: 10.1016/j.plaphy.2016.06.033
Zhang G. Y. Feng J. Wu J. Wang X. W. (2010). BoPMEI1, a pollen-specific pectin methylesterase inhibitor, has an essential role in pollen tube growth. Planta 231, 1323–1334. doi: 10.1007/s00425-010-1136-7
Zhang P. Wang H. Qin X. Chen K. Zhao J. Zhao Y. et al. (2019). Genome-wide identification, phylogeny and expression analysis of the PME and PMEI gene families in maize. Sci. Rep. 9, 19918. doi: 10.1038/s41598-019-56254-9
Zhao Y. Man Y. Wen J. Guo Y. Lin J. (2019). Advances in imaging plant cell walls. Trends Plant Sci. 482, 867–878. doi: 10.1016/j.tplants.2019.05.009