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Characterization of expansin genes and their transcriptional regulation by histone modifications in strawberry

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Abstract

Main conclusion

The possible candidate expansin genes, which may be important for strawberry fruit softening, have been identified in the diploid woodland strawberry Fragaria vesca and the octoploid cultivated strawberry Fragaria × ananassa and their transcriptional regulation by histone modifications has been studied.

Abstract

Softening process greatly affects fruit texture and shelf life. Expansins (EXPs) are a group of structural proteins participating in cell wall loosening, which break the hydrogen bonding between cellulose microfibrils and hemicelluloses. However, our knowledge on how EXP genes are regulated in fruit ripening, especially in non-climacteric fleshy fruits, is limited. Here, we have identified the EXP genes in both the octoploid cultivated strawberry (Fragaria × ananassa) and one of its diploid progenitor species, woodland strawberry (Fragaria vesca). We found that EXP proteins in F. × ananassa were structurally more divergent than the ones in F. vesca. Transcriptome data suggested that FaEXP88, FaEXP114, FveEXP11 and FveEXP33 were the four candidate EXP genes more likely involved in fruit softening, whose transcript levels dramatically increased when firmness decreased during fruit maturation. Phylogenetic analyses showed that those candidate genes were closely clustered, indicating the presence of homoeolog expression dominance in the EXP gene family in strawberry. Moreover, we have performed chromatin immunoprecipitation (ChIP) experiments to investigate the distribution of histone modifications along the promoters and genic regions of the EXP genes in F. vesca. ChIP data revealed that the transcript levels of EXP genes were highly correlated with the enrichment of H3K9/K14 acetylation and H3K27 tri-methylation. Collectively, this study identifies the key EXP genes involved in strawberry fruit softening and reveals a regulatory role of histone modifications in their transcriptional regulation, which would facilitate functional studies of the EXP genes in the ripening of non-climacteric fruits.

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Abbreviations

ChIP:

Chromatin immunoprecipitation

EXPA(B):

α-Expansin (ß-Expansin)

EXLA(B):

Expansin-like A(B)

References

  • Armenteros JJA, Tsirigos KD, Sonderby CK, Petersen TN, Winther O, Brunak S, von Heijne G, Nielsen H (2019) SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol 37:420–423

    Article  CAS  Google Scholar 

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202-208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brummell DA (2006) Cell wall disassembly in ripening fruit. Funct Plant Biol 33:103–119

    Article  CAS  PubMed  Google Scholar 

  • Brummell DA, Harpster MH, Civello PM, Bennett AB, Dunsmuir P (1999) Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell 11:2203–2216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools, a toolkit for biologists integrating various biological data handling tools with a user-friendly interface. Mol. Plant 13:1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Cheng J, Niu Q, Zhang B, Chen K, Yang R, Zhu JK, Zhang Y, Lang Z (2018) Downregulation of RdDM during strawberry fruit ripening. Genome Biol 19:212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Civello PM, Powell AL, Sabehat A, Bennett AB (1999) An expansin gene expressed in ripening strawberry fruit. Plant Physiol 121:1273–1279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coleman J, Inukai M, Inouye M (1985) Dual functions of the signal peptide in protein transfer across the membrane. Cell 43:351–360

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407:321–326

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ (2015) Plant expansins: diversity and interactions with plant cell walls. Curr Opin Plant Biol 25:162–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cosgrove DJ, Bedinger P, Durachko DM (1997) Group I allergens of grass pollen as cell wall-loosening agents. Plant Biol 94:6559–6564

    CAS  Google Scholar 

  • Crevillen P (2020) Histone demethylases as counterbalance to H3K27me3 silencing in plants. iScience 23:1–8

    Article  CAS  Google Scholar 

  • Dotto MC, Martinez GA, Civello PM (2006) Expression of expansin genes in strawberry varieties with contrasting fruit firmness. Plant Physiol Biochem 44:301–307

    Article  CAS  PubMed  Google Scholar 

  • Edger PP, Poorten TJ, VanBuren R, Hardigan MA, Colle M, McKain MR, Smith RD, Teresi SJ, Nelson ADL, Wai CM, Alger EI, Bird KA, Yocca AE, Pumplin N, Ou S, Ben-Zvi G, Brodt A, Baruch K, Swale T, Shiue L, Acharya CB, Cole GS, Mower JP, Childs KL, Jiang N, Lyons E, Freeling M, Puzey JR, Knapp SJ (2019) Origin and evolution of the octoploid strawberry genome. Nat Genet 51:541–547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fait A, Hanhineva K, Beleggia R, Dai N, Rogachev I, Nikiforova VJ, Fernie AR, Aharoni A (2008) Reconfifiguration of the achene and receptacle metabolic networks during strawberry fruit development. Plant Physiol 148:730–750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farinati S, Rasori A, Varotto S, Bonghi C (2017) Rosaceae fruit development, ripening and post-harvest: an epigenetic perspective. Front Plant Sci 8:1–14

    Article  Google Scholar 

  • Feng C, Wang J, Harris AJ, Folta KM, Zhao MZ, Kang M (2020) Tracing the diploid ancestry of the cultivated octoploid strawberry. Mol Biol Evol 38:478–485

    Article  PubMed Central  CAS  Google Scholar 

  • Figueroa CR, Pimentel P, Dotto MC, Civello PM, Martínez GA, Herrera R, Moya-León MA (2009) Expression of five expansin genes during softening of Fragaria chiloensis fruit: effect of auxin treatment. Postharvest Biol Technol 53:51–57

    Article  CAS  Google Scholar 

  • Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Res 32:D211-222

    Article  CAS  Google Scholar 

  • Furner IJ, Matzke M (2011) Methylation and demethylation of the Arabidopsis genome. Curr Opin Plant Biol 14:137–141

    Article  CAS  PubMed  Google Scholar 

  • Gallusci P, Hodgman C, Teyssier E, Seymour GB (2016) DNA methylation and chromatin regulation during fleshy fruit development and ripening. Front Plant Sci 7:1–14

    Article  Google Scholar 

  • Giovannoni J, Nguyen C, Ampofo B, Zhong S, Fei Z (2017) The epigenome and transcriptional dynamics of fruit ripening. Annu Rev Plant Biol 68:61–84

    Article  CAS  PubMed  Google Scholar 

  • Gu T, Jia S, Huang X, Wang L, Fu W, Huo G, Gan L, Ding J, Li Y (2019) Transcriptome and hormone analyses provide insights into hormonal regulation in strawberry ripening. Planta 250:145–162

    Article  CAS  PubMed  Google Scholar 

  • Han YC, Kuang JF, Chen JY, Liu XC, Xiao YY, Fu CC, Wang JN, Wu KQ, Lu WJ (2016) Banana transcription factor MaERF11 recruits histone deacetylase MaHDA1 and represses the expression of MaACO1 and expansins during fruit ripening. Plant Physiol 171:1070–1084

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison EP, McQueen-Mason SJ, Manning K (2001) Expression of six expansin genes in relation to extension activity in developing strawberry fruit. J Exp Bot 52:1437–1446

    Article  CAS  PubMed  Google Scholar 

  • Hollender CA, Kang C, Darwish O, Geretz A, Matthews BF, Slovin J, Alkharouf N, Liu Z (2014) Floral transcriptomes in woodland strawberry uncover developing receptacle and anther gene networks. Plant Physiol 165:1062–1075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang H, Liu R, Niu Q, Tang K, Zhang B, Zhang H, Chen K, Zhu JK, Lang Z (2019) Global increase in DNA methylation during orange fruit development and ripening. Proc Natl Acad Sci 116:1430–1436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X, Pan Q, Lin Y, Gu T, Li Y (2020) A native chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in strawberry fruits. Plant Methods 16:1–12

    Article  CAS  Google Scholar 

  • Jiang F, Lopez A, Jeon S, de Freitas ST, Yu Q, Wu Z, Labavitch JM, Tian S, Powell ALT, Mitcham E (2019) Disassembly of the fruit cell wall by the ripening-associated polygalacturonase and expansin influences tomato cracking. Hortic Res 6:1–15

    Article  CAS  Google Scholar 

  • Kang C, Darwish O, Geretz A, Shahan R, Alkharouf N, Liu Z (2013) Genome-scale transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca. Plant Cell 25:1960–1978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kende H, Bradford KJ, Brummell DA, Cho HT, Cosgrove DJ, Fleming AJ, Gehring C, Lee Y, McQueen-Mason S, Rose J, Voesenek LACJ (2004) Nomenclature for members of the expansin superfamily of genes and proteins. Plant Mol Biol 55:311–314

    Article  CAS  PubMed  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant elements and a portal to tools for promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Dai HY, Liu YX, Ma Y, Wu D, Zhang ZH (2015) A new strawberry cultivar ‘Yanli.’ Acta Hortic Sin 42:799–800

    Google Scholar 

  • Li D, Mou W, Xia R, Li L, Zawora C, Ying T, Mao L, Liu Z, Luo Z (2019) Integrated analysis of high-throughput sequencing data shows abscisic acid-responsive genes and miRNAs in strawberry receptacle fruit ripening. Hortic Res 6:26

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Liston A, Wei N, Tennessen JA, Li J, Dong M, Ashman TL (2020) Revisiting the origin of octoploid strawberry. Nat Genet 52:2–4

    Article  CAS  PubMed  Google Scholar 

  • McQueen-Mason SJ, Cosgrove DJ (1995) Expansin mode of action on cell walls. Plant Physiol 107:87–100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minoia S, Boualem A, Marcel F, Troadec C, Quemener B, Cellini F, Petrozza A, Vigouroux J, Lahaye M, Carriero F, Bendahmane A (2016) Induced mutations in tomato SlExp1 alter cell wall metabolism and delay fruit softening. Plant Sci 242:195–202

    Article  CAS  PubMed  Google Scholar 

  • Nardia CF, Villarreala NM, Dottoa MC, Arizad MT, Vallarinod JG, Martíneza GA, Valpuestad V, Civellob PM (2016) Influence of plant growth regulators on Expansin2 expression instrawberry fruit. Cloning and functional analysis of FaEXP2 promoter region. Postharvest Biol Technol 114:17–28

    Article  CAS  Google Scholar 

  • Pombo MA, Dotto MC, Martínez GA, Civello PM (2009) UV-C irradiation delays strawberry fruit softening and modifies the expression of genes involved in cell wall degradation. Postharvest Biol Technol 51:141–148

    Article  CAS  Google Scholar 

  • Qiao X, Li Q, Yin H, Qi K, Li L, Wang R, Zhang S, Paterson AH (2019) Gene duplication and evolution in recurring polyploidization-diploidization cycles in plants. Genome Biol 20:1–23

    Article  Google Scholar 

  • Sampedro J, Guttman M, Li LC, Cosgrove DJ (2015) Evolutionary divergence of beta-expansin structure and function in grasses parallels emergence of distinctive primary cell wall traits. Plant J 81:108–120

    Article  CAS  PubMed  Google Scholar 

  • Simithy J, Sidoli S, Yuan ZF, Coradin M, Bhanu NV, Marchione DM, Klein BJ, Bazilevsky GA, McCullough CE, Magin RS, Kutateladze TG, Snyder NW, Marmorstein R, Garcia BA (2017) Characterization of histone acylations links chromatin modifications with metabolism. Nat Commun 8:1–13

    Article  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Wang D, Xu W, Kong L, Ye X, Zhuang Q, Fan D, Luo K (2020) Histone methyltransferase ATX1 dynamically regulates fiber secondary cell wall biosynthesis in Arabidopsis inflorescence stem. Nucleic Acids Res 49:190–205

    Article  PubMed Central  Google Scholar 

  • Yang J, Liu D, Wang X, Ji C, Cheng F, Liu B, Hu Z, Chen S, Pental D, Ju Y, Yao P, Li X, Xie K, Zhang J, Wang J, Liu F, Ma W, Shopan J, Zheng H, Mackenzie SA, Zhang M (2016) The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection. Nat Genet 48:1225–1232

    Article  CAS  PubMed  Google Scholar 

  • Yennawar NH, Li LC, Dudzinski DM, Tabuchi A, Cosgrove DJ (2006) Crystal structure and activities of EXPB1 (Zea m 1), a beta-expansin and group-1 pollen allergen from maize. Proc Natl Acad Sci 103:14664–14671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Xu R, Gao Z, Chen C, Jiang Z, Shu H (2013) A genome-wide analysis of the expansin genes in Malus × Domestica. Mol Genet Genom 289:225–236

    Article  CAS  Google Scholar 

  • Zhang SW, Zhang TH, Zhang JN, Huang Y (2014) Prediction of signal peptide cleavage sites with subsite-coupled and template matching fusion algorithm. Mol Inform 23:230–239

    Article  CAS  Google Scholar 

  • Zheng M, Liu X, Lin J, Liu X, Wang Z, Xin M, Yao Y, Peng H, Zhou DX, Ni Z, Sun Q, Hu Z (2019) Histone acetyltransferase GCN5 contributes to cell wall integrity and salt stress tolerance by altering the expression of cellulose synthesis genes. Plant J 97:587–602

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Dr. Xin Qiao and Yang Yuan for technical support for the bioinformatic analysis. This work was supported by the National Natural Science Foundation of China (31972382 to TG).

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This work was supported by the National Natural Science Foundation of China (31972382 to TG).

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Correspondence to Yi Li or Tingting Gu.

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Mu, Q., Li, X., Luo, J. et al. Characterization of expansin genes and their transcriptional regulation by histone modifications in strawberry. Planta 254, 21 (2021). https://doi.org/10.1007/s00425-021-03665-6

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