Browse > Article
http://dx.doi.org/10.5010/JPB.2022.49.4.271

Genome-wide identification and expression profiling of the pectin methylesterase gene family in Citrus sinensis (L.) Osbeck  

Ho Bang Kim (Life Sciences Research Institute, Biomedic Co., Ltd.)
Chang Jae Oh (Life Sciences Research Institute, Biomedic Co., Ltd.)
Nam-Hoon Kim (PHYZEN Genomics Institute)
Cheol Woo Choi (Citrus Research Institute, National Institute of Horticultural & Herbal Science)
Minju Kim (Citrus Research Institute, National Institute of Horticultural & Herbal Science)
Sukman Park (Citrus Research Institute, National Institute of Horticultural & Herbal Science)
Seong Beom Jin (Citrus Research Institute, National Institute of Horticultural & Herbal Science)
Su-Hyun Yun (Citrus Research Institute, National Institute of Horticultural & Herbal Science)
Kwan Jeong Song (Major of Horticultural Science, Faculty of Bioscience and Industry, Jeju National University)
Publication Information
Journal of Plant Biotechnology / v.49, no.4, 2022 , pp. 271-291 More about this Journal
Abstract
Pectin methylesterase (PME) plays an important role in vegetative and reproductive development and biotic/abiotic stress responses by regulating the degree of methyl-esterification of pectic polysaccharides in the plant cell wall. PMEs are encoded by a large multigene family in higher land plant genomes. In general, the expression of plant PME genes shows tissue- or cell-specific patterns and is induced by endogenous and exogenous stimuli. In this study, we identified PME multigene family members (CsPMEs) from the sweet orange genome and report detailed molecular characterization and expression profiling in different citrus tissues and two fruit developmental stages. We also discussed the possible functional roles of some CsPME genes by comparing them with the known functions of PMEs from other plant species. We identified 48 CsPME genes from the citrus genome. A phylogenetic tree analysis revealed that the identified CsPMEs were divided into two groups/types. Some CsPMEs showed very close phylogenetic relationships with the PMEs whose functions were formerly addressed in Arabidopsis, tomato, and maize. Expression profiling showed that some CsPME genes are highly or specifically expressed in the leaf, root, flower, or fruit. Based on the phylogenetic relationships and gene expression profiling results, we suggest that some CsPMEs could play functional roles in pollen development, pollen tube growth, cross incompatibility, root development, embryo/seed development, stomata movement, and biotic/abiotic stress responses. Our results shed light on the biological roles of individual CsPME isoforms and contribute to the search for genetic variations in citrus genetic resources.
Keywords
Citrus; Genome; Multigene Family; Pectin Methylesterase; Plant Cell Wall; Transcriptome;
Citations & Related Records
Times Cited By KSCI : 7  (Citation Analysis)
연도 인용수 순위
1 Woo J-K, Yun S-H, Yi KU, Park YC, Lee H-Y, Kim M, Lee Y, Song KJ, Kim HB (2020) Identification of citrus varieties bred in Korea using microsatellite markers. Hortic Sci Technol 38:374-384
2 Wu H-C, Bulgakov VP, Jinn T-L (2018) Pectin methylesterases: cell wall remodeling proteins are required for plant response to heat stress. Front Plant Sci 9:1612
3 Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C et al. (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59-66   DOI
4 Zhang P, Wang H, Qin X, Chen K, Zhao J, Zhao Y, Yue B (2019) Genome-wide identifcation, phylogeny and expression analysis of the PME and PMEI gene families in maize. 9:19918
5 Zhang Z, Zhang B, Chen Z, Zhang D, Zhang H, Wang H et al (2018) A PECTIN METHYLESTERASE gene at the maize Ga1 locus confers male function in unilateral cross-incompatibility. Nat Commun 9:3678 
6 Amos RA, Pattathil S, Yang JY, Atmodjo MA, Urbanowicz BR, Moremen KW, Mohnen D (2018) A two-phase model for the non-processive biosynthesis of homogalacturonan polysaccharides by the GAUT1:GAUT7 complex. J Biol Chem 293:19047-19063
7 Amsbury S, Hunt L, Elhaddad N, Baillie A, Lundgren M, Verhertbruggen Y, Scheller HV, J. Paul Knox JP, Fleming AJ, Gray JE (2016) Stomatal function requires pectin de-methyl-esterification of the guard cell wall. Current Biol 26:2899-2906   DOI
8 Atmodjo MA, Sakuragi Y, Zhu X, Burrell AJ, Mohanty SS, Atwood JA 3rd, Orlando R, Scheller HV, Mohnen D (2011) Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan: galacturonosyltransferase complex. Proc Natl Acad Sci USA 108:20225-20230   DOI
9 Dorokhov YL, Skurat EV, Frolova OY, Gasanova TV, Ivanov PA, Ravin NV, Skryabin KG, Makinen KM, Klimyuk VI, Gleba YY, Atabekov JG (2006) Role of the leader sequence in tobacco pectin methylesterase secretion. FEBS Lett 580:3329-3334   DOI
10 Eddy SR, Pearson WR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7:e1002195
11 Francis KE, Lam SY, Copenhaver GP (2006) Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiol 142:1004-1013   DOI
12 Geisler-Lee J, Geisler M, Coutinho PM, Segerman B, Nishikubo N, Takahashi J, Aspeborg H, Djerbi S, Master E, Andersson-Gunneras S, Sundberg B, Karpinski S, Teeri TT, Kleczkowski LA, Henrissat B, Mellerowicz EJ (2006) Poplar carbohydrate-active enzymes. Gene identification and expression analyses. Plant Physiol 140:946-962   DOI
13 Gmitter FG, Chen C, Machado MA, de Souza AA, Ollitrault P, Froehlicher Y, Shimizu (2012) Citrus genomics. Tree Genet Genomes 8:611-626   DOI
14 Huang Y-C, Hui-Chen Wu H-C, Wang Y-D, Liu C-H, Lin C-C, Luo D-L, Jinn T-L (2017) PECTIN METHYLESTERASE34 contributes to heat tolerance through its role in promoting stomatal movement. Plant Physiol 174:748-763   DOI
15 Guenin S, Mareck A, Rayon C, Lamour R, Assoumou Ndong Y, Domon JM, Senechal F, Fournet F, Jamet E, Canut H, Percoco G, Mouille G, Rolland A, Rusterucci C, Guerineau F, Van Wuytswinkel O, Gillet F, Driouich A, Lerouge P, Gutierrez L, Pelloux J (2011) Identification of pectin methylesterase 3 as a basic pectin methylesterase isoform involved in adventitious rooting in Arabidopsis thaliana. New Phytol 192:114-126   DOI
16 Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ (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
17 Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296-1297   DOI
18 Jeong HY, Nguyen HP, 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 183:23-29   DOI
19 Jiang L, Yang SL, Xie LF, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584-96   DOI
20 Kim HB, Jun S-S, Choe S, Cho JY, Choi S-B, Kim S-C (2010) Identification of differentially expressed genes from male and female flowers of kiwifruit. Afr J Biotechnol 9:6684-6694
21 Kim HB, Kim JJ, Oh CJ, Yun S-H, Song KJ (2016) Current status and prospects of molecular marker development for systematic breeding program in citrus. J Plant Biotechnol 43:261-271   DOI
22 Levesque-Tremblay G, Muller K, Mansfield SD, Haughn GW (2015) HIGHLY METHYL ESTERIFIED SEEDS is a pectin methyl esterase involved in embryo development. Plant Physiol 167:725-737
23 Kim S-C, Uhm YK, Ko S, Oh CJ, Kwack Y-B, Kim HL, Lee Y, An CS, Park PB, Kim HB (2015) KiwiPME1 encoding pectin methylesterase is specifically expressed in the pollen of a dioecious plant species, kiwifruit (Actinidia chinensis). Hort Environ Biotechnol 56:402-410
24 Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870-1874   DOI
25 Leroux C, Bouton S, Kiefer-Meyer M-C, Fabrice TN, Mareck A, Guenin S, Fournet F, Ringli C, Pelloux J, Driouich A, Lerouge P, Lehner A, Mollet J-C (2015) PECTIN METHYLESTERASE48 is involved in Arabidopsis pollen grain germination. Plant Physiol 167:367-380
26 Liu H, Lyu H-M, Zhu K, de Peer YV, Cheng Z-M (2021) The emergence and evolution of intron-poor and intronless genes in intron-rich plant gene families. Plant J 105:1072-1082   DOI
27 Louvet R, Cavel E, Gutierrez L, Guenin S, Roger D, Gillet F, Guerineau F, Pelloux J (2006) Comprehensive expression profiling of the pectin methylesterase gene family during silique development in Arabidopsis thaliana. Planta 224:782-791   DOI
28 Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550
29 Markovic O, Janecek S (2004) Pectin methylesterases: sequence-structural features and phylogenetic relationships. Carbohydrate Res 339:2281-2295   DOI
30 Micheli F (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:414-418   DOI
31 Phan TD, Bo W, West G, Lycett GW, Tucker GA (2007) Silencing of the major salt-dependent isoform of pectinesterase in tomato alters fruit softening. Plant Physiol 144:1960-1967   DOI
32 Moller S, Croning MDR, Apweiler R (2001) Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17:646-653   DOI
33 Moran Lauter AN, Muszynski MG, Huffman RD, Scott MP (2017) A Pectin methylesterase ZmPme3 is expressed in gametophyte factor1-s (Ga1-s) silks and maps to that locus in maize (Zea mays L.). Front Plant Sci 8:1926
34 Pelloux J, Rusterucci C, Mellerowicz E (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12:267-277   DOI
35 Pok P, Oh E, Yi K, Kang JH, Ko BY, Kim HB, Song KJ (2015) Characterization of microspore development and pollen tube growth response to self- and cross-pollination in Jeju old local citrus species. Hort Environ Biotechnol 56:225-232.   DOI
36 Putri G, Anders S, Pyl PT, Pimanda JE, Zanini F (2022) Analysing high-throughput sequencing data in Python with HTSeq 2.0. Bioinformatics 38:2943-2945   DOI
37 Raiola A, Lionetti V, Elmaghraby I, Immerzeel P, Mellerowicz EJ, Salvi G, Cervone F, Bellincampi D (2011). Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Mol Plant Microbe Interact 24:432-40   DOI
38 Rogozin IB, Carmel L, Csuros M, Koonin EV (2012) Origin and evolution of spliceosomal introns. Biol Direct 7:11
39 Ruiz-May E, Kim S-J, Brandizzi F, Rose JKC (2012) The secreted plant N-glycoproteome and associated secretory pathways. Front Plant Sci 3:117
40 Senechal F, Graff L, Surcouf O, Marcelo P, Rayon C, Bouton S, Mareck A, Mouille G, Stintzi A, Hofte H, Lerouge P, Schaller A, Pelloux J (2014a) Arabidopsis PECTIN METHYLESTERASE17 is co-expressed with and processed by SBT3.5, a subtilisin-like serine protease. Ann Bot 114:1161-1175   DOI
41 Senechal F, Wattier C, Rusterucci C, Pelloux J (2014b) Homogalacturonan-modifying enzymes: structure, expression, and roles in plants. J Exp Bot 65:5125-5160   DOI
42 Simons H, Tucker GA (1999) Simultaneous co-suppression of polygalacturonase and pectinesterase in tomato fruit: inheritance and effect on isoform profiles. Phytochem 52:1017-1022   DOI
43 Teufel F, Almagro Armenteros JJ, Johansen AR, Gislason MH, Pihl SI, Tsirigos KD, Winther O, Brunak S, von Heijne G, Nielsen H (2022) SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat Biotechnol https://doi.org/10.1038/s41587-021-01156-3   DOI
44 Tian GW, Chen MH, Zaltsman A, Citovsky V (2006) Pollen-specific pectin methylesterase involved in pollen tube growth. Dev Biol 294:83-91   DOI
45 Tieman DM, Harriman RW, Ramamohan G, Handa AK (1992) An antisense pectin methylesterase gene alters pectin chemistry and soluble solids in tomato fruit. Plant Cell 4:667-679   DOI
46 Turbant A, Fournet F, Lequart M, Zabijak L, Pageau K, Bouton S, Van Wuytswinkel O (2016) PME58 plays a role in pectin distribution during seed coat mucilage extrusion through homogalacturonan modification. J Exp Bot 67:2177-2190   DOI
47 Wang D, Yeats TH, Uluisik S, Rose JKC, Seymour GB (2018) Fruit softening: Revisiting the role of pectin. Trends Plant Sci 23:302-310   DOI
48 Wang L, Gao Y, Wang S, Zhang Q, Yang S (2021) Genome-wide identifcation of PME genes, evolution and expression analyses in soybean (Glycine max L.). BMC Plant Biol 21:578.
49 Wen B, Strom A, Tasker A, West G, Tucker GA (2013) Effect of silencing the two major tomato fruit pectin methylesterase isoforms on cell wall pectin metabolism. Plant Biol 15:1025-1032   DOI
50 Wang Y, Li W, Wang L, Yan J, Lu G, Yang N, Xu J, Wang Y, Gui S, Chen G, Li S, Wu C, Guo T, Xiao Y, Warburton ML, Fernie AR, Dresselhaus T, Yan J (2022) Three types of genes underlying the Gametophyte factor1 locus cause unilateral cross incompatibility in maize. Nat Commun 13:4498
51 Wen B, Zhang F, Wu X, Li H (2020) Characterization of the tomato (Solanum lycopersicum) pectin methylesterases: evolution, activity of isoforms and expression during fruit ripening. Front Plant Sci 11:238
52 Wolf S, Greiner S (2012) Growth control by cell wall pectins. Protoplasma 249:S169-S175
53 Wolf S, Mouille G, Pelloux J (2009) Homogalacturonan methyl-esterification and plant development. Mol Plant 2:851-860   DOI