Genome-wide analysis of the PME gene family reveals its role in suppressing fruit lignification in pear

Fanhang Zhang1(), Qi Wang1(), Kaili Yuan1(), Zhihua Xie1(), Kaijie Qi1(), Wen Li1(), Xin Gong1(), Shaoling Zhang1(), Shutian Tao1()()

PDF
Horticulture Advances ›› 2024, Vol. 2 ›› Issue (1) : 9. DOI: 10.1007/s44281-024-00033-8

Genome-wide analysis of the PME gene family reveals its role in suppressing fruit lignification in pear

  • Fanhang Zhang1(), Qi Wang1(), Kaili Yuan1(), Zhihua Xie1(), Kaijie Qi1(), Wen Li1(), Xin Gong1(), Shaoling Zhang1(), Shutian Tao1()()
Author information +
History +

Abstract

In pears, the presence of stone cells adversely affects fruit quality. Pectin methylesterase (PME) plays various roles in plant biology, including lignin biosynthesis. However, only a limited fraction has been functionally characterized, and the distribution and function of PME in many Rosaceae trees remain unexplored. In this study, we identified 396 putative PME family candidate genes, with 81 in Pyrus bretschneideri, 92 in Malus domestica, 62 in Fragaria vesca, 65 in Prunus mume, 15 in Pyrus communis, and 81 in Pyrus pyrifolia. Leveraging insights from model plants, we categorized PME family genes into four groups. Additionally, the evolution of the PME gene family was shaped by various gene duplication events, primarily dispersed duplication, influenced by purifying selection. A specific gene, Pbr031522.1, designated PbPME35, emerged as a candidate associated with lignin biosynthesis in pear fruits, supported by RNA-seq data. The role of PbPME35 in repressing lignification was validated through its overexpression in pear callus and Arabidopsis. Overall, our findings highlight the ability of PbPME35 to reduce lignin content in pear fruit by downregulating the expression levels of lignin biosynthesis genes. These findings provide new insights into the characteristics of PME genes and their role in regulating lignification in pear fruits.

Keywords

Pear / Stone cell / Lignin biosynthesis / Pectin methylesterase

Cite this article

Download citation ▾
Fanhang Zhang, Qi Wang, Kaili Yuan, Zhihua Xie, Kaijie Qi, Wen Li, Xin Gong, Shaoling Zhang, Shutian Tao. Genome-wide analysis of the PME gene family reveals its role in suppressing fruit lignification in pear. Horticulture Advances, 2024, 2(1): 9 https://doi.org/10.1007/s44281-024-00033-8

References

[1]
Bai S, Tao R, Tang Y, Yin L, Ma Y, Ni J, et al. BBX16, a B-box protein, positively regulates light-induced anthocyanin accumulation by activating MYB10 in red pear. Plant Biotechnol J. 2019;17:1985–97. https://doi.org/10.1111/pbi.13114.
[2]
Bailey TL, Bodén M, Whitington T, Machanick P. The value of position-specific priors in motif discovery using MEME. BMC Bioinf. 2010;11:179. https://doi.org/10.1186/1471-2105-11-179.
[3]
Carpin S, Crèvecoeur M, de Meyer M, Simon P, Greppin H, Penel C. Identification of a Ca2+-pectate binding site on an apoplastic peroxidase. Plant Cell. 2001;13:511–20. https://doi.org/10.1105/tpc.13.3.511.
[4]
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020;13:1194–202. https://doi.org/10.1016/j.molp.2020.06.009.
[5]
Daccord N, Celton JM, Linsmith G, Becker C, Choisne N, Schijlen E, et al. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nature Genet. 2017;49:1099–106. https://doi.org/10.1038/ng.3886.
[6]
Dunand C, Tognolli M, Overney S, von Tobel L, de Meyer M, Simon P, et al. Identification and characterisation of Ca2+-pectate binding peroxidases in Arabidopsis thaliana. J Plant Physiol. 2002;159:1165–71. https://doi.org/10.1078/0176-1617-00768.
[7]
Fawcett JA, Maere S, Van De Peer Y. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc Natl Acad Sci USA. 2009;106:5737–42. https://doi.org/10.1073/pnas.0900906106.
[8]
Freeling M. Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol. 2009;60:433–53. https://doi.org/10.1146/annurev.arplant.043008.092122.
[9]
Fry SC. Primary cell wall metabolism: tracking the careers of wall polymers in living plant cells. New Phytol. 2004;161:641–75. https://doi.org/10.1111/j.1469-8137.2004.00980.x.
[10]
Gao Y, Yang Q, Yan X, Wu X, Yang F, Li J, et al. High-quality genome assembly of “Cuiguan” pear (Pyrus pyrifolia) as a reference genome for identifying regulatory genes and epigenetic modifications responsible for bud dormancy. Hortic Res. 2021;8:197. https://doi.org/10.1038/s41438-021-00632-w.
[11]
Geisler-Lee J, Geisler M, Coutinho PM, Segerman B, Nishikubo N, Takahashi J, et al. Poplar carbohydrate-active enzymes. Gene identification and expression analyses. Plant Physiol. 2006;140:946–62. https://doi.org/10.1104/pp.105.072652.
[12]
Gong X, Qi K, Chen J, Zhao L, Xie Z, Yan X, et al. Multi-omics analyses reveal the difference of stone cell distribution in pear fruit. Plant J. 2022;113:626–42. https://doi.org/10.1111/tpj.16073.
[13]
Gong X, Xie Z, Qi K, Zhao L, Yuan Y, Xu J, et al. PbMC1a/1b regulates lignification during stone cell development in pear (Pyrus bretschneideri) fruit. Hortic Res. 2020;7:59. https://doi.org/10.1038/s41438-020-0280-x.
[14]
Guglielmino N, Liberman M, Catesson A, Mareck A, Prat R, Mutaftschiev S, et al. Pectin methylesterases from poplar cambium and inner bark: localization, properties and seasonal changes. Planta. 1997;202:70–5. https://doi.org/10.1007/s004250050104.
[15]
He Y, Bose SK, Wang W, Jia X, Lu H, Yin H. Pre-harvest treatment of chitosan oligosaccharides improved strawberry fruit quality. Int J Mol Sci. 2018;19:2194. https://doi.org/10.3390/ijms19082194.
[16]
Hertzberg M, Aspeborg H, Schrader J, Andersson A, Erlandsson R, Blomqvist K, et al. A transcriptional roadmap to wood formation. Proc Natl Acad Sci USA. 2001;98:14732–7. https://doi.org/10.1073/pnas.261293398.
[17]
Hu Y, Cheng H, Zhang Y, Zhang J, Niu S, Wang X, et al. The MdMYB16/MdMYB1-miR7125-MdCCR module regulates the homeostasis between anthocyanin and lignin biosynthesis during light induction in apple. New Phytol. 2021;231:1105–22. https://doi.org/10.1111/nph.17431.
[18]
Huang W, Shi Y, Yan H, Wang H, Wu D, Grierson D, et al. The calcium-mediated homogalacturonan pectin complexation in cell walls contributes the firmness increase in loquat fruit during postharvest storage. J Adv Res. 2022;49:47–62. https://doi.org/10.1016/j.jare.2022.09.009.
[19]
Huang X, Li K, Xu X, Yao Z, Jin C, Zhang S. Genome-wide analysis of WRKY transcription factors in white pear (Pyrus bretschneideri) reveals evolution and patterns under drought stress. BMC Genomics. 2015;16:1–14. https://doi.org/10.1186/s12864-015-2233-6.
[20]
Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, et al. Ancestral polyploidy in seed plants and angiosperms. Nature. 2011;473:97–100. https://doi.org/10.1038/nature09916.
[21]
Jolie RP, Duvetter T, Van Loey AM, Hendrickx ME. Pectin methylesterase and its proteinaceous inhibitor: a review. Carbohydr Res. 2010;345:2583–95. https://doi.org/10.1016/j.carres.2010.10.002.
[22]
Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings Bioinf. 2019;20:1160–6. https://doi.org/10.1093/bib/bbx108.
[23]
Lairez D, Cathala B, Monties B, Bedos-Belval F, Duran H, Gorrichon L. Aggregation during coniferyl alcohol polymerization in pectin solution: a biomimetic approach of the first steps of lignification. Biomacromol. 2005;6:763–74. https://doi.org/10.1021/bm049390y.
[24]
Levesque-Tremblay G, Müller K, Mansfield SD, Haughn GW. Highly methyl esterified seeds is a pectin methyl esterase involved in embryo development. Plant Physiol. 2015;167:725–37. https://doi.org/10.1104/pp.114.255604.
[25]
Li Y, Pi M, Gao Q, Liu Z, Kang C. Updated annotation of the wild strawberry Fragaria vesca V4 genome. Hortic Res. 2019;6:61. https://doi.org/10.1038/s41438-019-0142-6.
[26]
Linsmith G, Rombauts S, Montanari S, Deng CH, Celton J-M, Guérif P, et al. Pseudo-chromosome–length genome assembly of a double haploid “Bartlett” pear (Pyrus communis L.). Gigascience. 2019;8:giz138. https://doi.org/10.1093/gigascience/giz138.
[27]
Louvet R, Cavel E, Gutierrez L, Guénin S, Roger D, Gillet F, et al. Comprehensive expression profiling of the pectin methylesterase gene family during silique development in Arabidopsis thaliana. Planta. 2006;224:782–91. https://doi.org/10.1007/s00425-006-0261-9.
[28]
Lu S, Wang J, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, et al. CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res. 2020;48:D265–8. https://doi.org/10.1093/nar/gkz991.
[29]
Lynch M, Force A. The probability of duplicate gene preservation by subfunctionalization. Genetics. 2000;154:459–73. https://doi.org/10.1093/genetics/154.1.459.
[30]
McCarthy RL, Zhong R, Ye ZH. MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell Physiol. 2009;50:1950–64. https://doi.org/10.1093/pcp/pcp139.
[31]
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, Von Haeseler A, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37:1530–4. https://doi.org/10.1093/molbev/msaa015.
[32]
Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M. The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell. 2005;17:2993–3006. https://doi.org/10.1105/tpc.105.036004.
[33]
?hman D, Demedts B, Kumar M, Gerber L, Gorzsás A, Goeminne G, et al. MYB103 is required for FERULATE-5-HYDROXYLASE expression and syringyl lignin biosynthesis in Arabidopsis stems. Plant J. 2013;73:63–76. https://doi.org/10.1111/tpj.12018.
[34]
Pelletier S, Van Orden J, Wolf S, Vissenberg K, Delacourt J, Ndong YA, et al. A role for pectin de-methylesterification in a developmentally regulated growth acceleration in dark-grown Arabidopsis hypocotyls. New Phytol. 2010;188:726–39. https://doi.org/10.1111/j.1469-8137.2010.03409.x.
[35]
Pelloux J, Rusterucci C, Mellerowicz EJ. New insights into pectin methylesterase structure and function. Trends Plant Sci. 2007;12:267–77. https://doi.org/10.1016/j.tplants.2007.04.001.
[36]
Qiao X, Li M, Li L, Yin H, Wu J, Zhang S. Genome-wide identification and comparative analysis of the heat shock transcription factor family in Chinese white pear (Pyrus bretschneideri) and five other Rosaceae species. BMC Plant Biol. 2015;15:12. https://doi.org/10.1186/s12870-014-0401-5.
[37]
Qiao X, Li Q, Yin H, Qi K, Li L, Wang R, et al. Gene duplication and evolution in recurring polyploidization–diploidization cycles in plants. Genome Biol. 2019;20:38. https://doi.org/10.1186/s13059-019-1650-2.
[38]
R?ckel N, Wolf S, Kost B, Rausch T, Greiner S. Elaborate spatial patterning of cell-wall PME and PMEI at the pollen tube tip involves PMEI endocytosis, and reflects the distribution of esterified and de-esterified pectins. Plant J. 2008;53:133–43. https://doi.org/10.1111/j.1365-313X.2007.03325.x.
[39]
Sexton TR, Henry RJ, Harwood CE, Thomas DS, McManus LJ, Raymond C, et al. Pectin methylesterase genes influence solid wood properties of Eucalyptus pilularis. Plant Physiol. 2012;158:531–41. https://doi.org/10.1104/pp.111.181602.
[40]
Tang C, Zhu X, Qiao X, Gao H, Li Q, Wang P, et al. Characterization of the pectin methyl-esterase gene family and its function in controlling pollen tube growth in pear (Pyrus bretschneideri). Genomics. 2020;112:2467–77. https://doi.org/10.1016/j.ygeno.2020.01.021.
[41]
Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH. Synteny and collinearity in plant genomes. Science. 2008;320:486–8. https://doi.org/10.1126/science.1153917.
[42]
Tao S, Khanizadeh S, Zhang H, Zhang S. Anatomy, ultrastructure and lignin distribution of stone cells in two Pyrus species. Plant Sci. 2009;176:413–9. https://doi.org/10.1016/j.plantsci.2008.12.011.
[43]
Wang R, Xue Y, Fan J, Yao JL, Qin M, Lin T, et al. A systems genetics approach reveals PbrNSC as a regulator of lignin and cellulose biosynthesis in stone cells of pear fruit. Genome Biol. 2021;22:313. https://doi.org/10.1186/s13059-021-02531-8.
[44]
Wen B, Zhang F, Wu X, Li H. Characterization of the tomato (Solanum lycopersicum) pectin methylesterases: evolution, activity of isoforms and expression during fruit ripening. Front Plant Sci. 2020;11:238. https://doi.org/10.3389/fpls.2020.00238.
[45]
Wi S, Singh A, Lee K, Kim Y. The pattern of distribution of pectin, peroxidase and lignin in the middle lamella of secondary xylem fibres in alfalfa (Medicago sativa). Ann Bot. 2005;95:863–8. https://doi.org/10.1093/aob/mci092.
[46]
Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, et al. The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res. 2013;23:396–408. https://doi.org/10.1101/gr.144311.112.
[47]
Xue C, Guan SC, Chen JQ, Wen CJ, Cai JF, Chen X. Genome wide identification and functional characterization of strawberry pectin methylesterases related to fruit softening. BMC Plant Biol. 2020;20:13. https://doi.org/10.1186/s12870-019-2225-9.
[48]
Xue C, Yao JL, Xue YS, Su GQ, Wang L, Lin LK, et al. PbrMYB169 positively regulates lignification of stone cells in pear fruit. J Exp Bot. 2019;70:1801–14. https://doi.org/10.1093/jxb/erz039.
[49]
Yang Y, Li R, Qi M. In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves. Plant J. 2000;22:543–51. https://doi.org/10.1046/j.1365-313x.2000.00760.x.
[50]
Zhang F, Lu K, Gu Y, Zhang L, Li W, Li Z. Effects of low-temperature stress and brassinolide application on the photosynthesis and leaf structure of tung tree seedlings. Front Plant Sci. 2020;10:1767. https://doi.org/10.3389/fpls.2019.01767.
[51]
Zhang MY, Xue C, Hu H, Li J, Xue Y, Wang R, et al. Genome-wide association studies provide insights into the genetic determination of fruit traits of pear. Nature Commun. 2021;12:1144. https://doi.org/10.1038/s41467-021-21378-y.
[52]
Zhang Q, Chen W, Sun L, Zhao F, Huang B, Yang W, et al. The genome of Prunus mume. Nat Commun. 2012;3:1318. https://doi.org/10.1038/ncomms2290.
[53]
Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH. A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell. 2008;20:2763–82. https://doi.org/10.1105/tpc.108.061325.
[54]
Zhou J, Lee C, Zhong R, Ye ZH. MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell. 2009;21:248–66. https://doi.org/10.1105/tpc.108.063321.
Funding
Jiangsu Provincial Key Research and Development Program(BE2023365); National Natural Science Foundation of China(U2003121); Jiangsu Agriculture Science and Technology Innovation Fund(CX(22)2025); Achievement Transformation Fund Project of Sanya Institute of Nanjing Agricultural University(NAUSY-CG-YB06)
PDF

Accesses

Citations

Detail

Sections
Recommended

/