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Differentially expressed genes related to the formation of russet fruit skin in a mutant of ‘Dangshansuli’ pear (Pyrus bretchnederi Rehd.) determined by suppression subtractive hybridization

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Abstract

The mature fruit skin of ‘Dangshansuli’ pear (Pyrus bretchnederi Rehd.) is yellow-green, but the fruit of the mutant, ‘Xiusu’, is russetted. To understand the mechanism of russet formation, the suppression subtractive hybridization libraries were used to screen for differentially expressed genes between the wild type pear and the mutant. Three hundred and twenty nine and 366 unigenes were obtained from 934 and 929 colonies in the forward and reverse libraries, respectively. The results indicated that phenylpropanoid metabolism, ethylene metabolism and secondary metabolism might be involved in the russet formation process, and fruit skin is likely to be regulated by lignin synthesis, polyamine and H2O2 signalling. Furthermore, the accumulation of lignin and H2O2, together with up-regulated POD enzyme genes expression in the exocarp of ‘Xiusu’ compare with ‘Dangshansuli’ pear control, provided a comprehensive transcriptomics view on the coordination of the russet formation of mutant pear.

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Abbreviations

bHLH:

Basic helix-loop-helix

CCoAOMT:

Caffeoyl coenzyme A O-methyltransferase

COMT:

Caffeic acid O-methyltransferase

DAFB:

Day after full bloom

EG:

Endo-1,4-beta-d-glucanase

ISSR:

Inter-simple sequence repeat

PCR:

Polymerase chain reaction

RAPD:

Randomly amplified polymorphic DNA

SAMDC:

S-adenosylmethionine decarboxylase

SAMS:

S-adenosyl-l-methionine synthetase

SSH:

Suppression subtractive hybridization

TEM:

Transmission electron microscopy

XTH:

Xyloglucan endotransglucosylase/hydrolase

References

  • Chatelet P, Laucou V, Fernandez L, Sreekantan L, Lacombe T, Martinez-Zapater JM, Thomas MR, Torregrosa L (2007) Characterization of Vitis vinifera L. somatic variants exhibiting abnormal flower development patterns. J Exp Bot 58:4107–4118

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dondini L, Pierantoni L, Ancarani V, D’Angelo M, Cho KH, Shin IS, Musacchi S, Kang SJ, Sansavini S (2008) The inheritance of the red color character in European pear (Pyrus communis) and its map position in the mutated cultivar ‘Max Red Bartlett’. Plant Breed 127:524–526

    Article  Google Scholar 

  • Egusa M, Ochi H, Tsuge T, Otani H, Kodama M (2009) Identification of putative defense-related genes in Japanese pear against Alternaria alternata infection using suppression subtractive hybridization and expression analysis. J Gen Plant Pathol 75:119–124

    Article  CAS  Google Scholar 

  • Fornale S, Shi XH, Chai CL, Encina A, Irar S, Capellades M, Fuguet E, Torres JL, Rovira P, Puigdomenech P, Rigau J, Grotewold E, Gray J, Caparros-Ruiz D (2010) ZmMYB31 directly represses maize lignin genes and redirects the phenylpropanoid metabolic flux. Plant J 64:633–644

    Article  CAS  PubMed  Google Scholar 

  • Ge XX, Chai LJ, Liu Z, Wu XM, Deng XX, Guo WW (2012) Transcriptional profiling of genes involved in embryogenic, non-embryogenic calluses and somatic embryogenesis of Valencia sweet orange by SSH-based microarray. Planta 236:1107–1124

    Article  CAS  PubMed  Google Scholar 

  • Gil-Amado JA, Gomez-Jimenez MC (2012) Regulation of polyamine metabolism and biosynthetic gene expression during olive mature-fruit abscission. Planta 235:1221–1237

    Article  CAS  PubMed  Google Scholar 

  • Goujon T, Minic Z, Amrani AE, Lerouxel O, Aletti E, Lapierre C, Joseleau JP, Jouanin L (2003) AtBXL1, a novel higher plant (Arabidopsis thaliana) putative beta-xylosidase gene, is involved in secondary cell wall metabolism and plant development. Plant J 33:77–690

    Article  Google Scholar 

  • Inoue E, Kasumi M, Sakuma F, Anzai H, Amano K, Hara H (2006) Identification of RAPD marker linked to fruit skin color in Japanese pear (Pyrus pyrifolia Nakai). Sci Hortic Amsterdam 107:254–258

    Article  CAS  Google Scholar 

  • Kobayashi S, Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304:982

    Article  PubMed  Google Scholar 

  • Leida C, Terol J, Marti G, Agusti M, Llacer G, Badenes ML, Rios G (2010) Identification of genes associated with bud dormancy release in Prunus persica by suppression subtractive hybridization. Tree Physiol 30:655–666

    Article  CAS  PubMed  Google Scholar 

  • Li XF, Li X, Jia B, Liu L, Ye ZF, Heng W, Zhu LW (2012) Analysis of enzyme activity and lignin content and expression of CCoAOMT gene in the exocarp of ‘Dangshansuli’ and its russet mutant. Acta Hortic Sinica 39:828–836

    CAS  Google Scholar 

  • Liu Q, Zhu AD, Chai LJ, Zhou WJ, Yu KQ, Ding J, Xu J, Deng XX (2009) Transcriptome analysis of a spontaneous mutant in sweet orange [Citrus sinensis (L.) Osbeck] during fruit development. J Exp Bot 60:801–813

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu SM, Song J, Campbell-Palmer L (2009) A modified chemiluminescence method for hydrogen peroxide determination in apple fruit tissues. Sci Hortic Amsterdam 120:336–341

    Article  CAS  Google Scholar 

  • Malladi A, Hirst PM (2010) Increase in fruit size of a spontaneous mutant of ‘Gala’ apple (Malus × domestica Borkh.) is facilitated by altered cell production and enhanced cell size. J Exp Bot 61:3003–3013

    Article  CAS  PubMed  Google Scholar 

  • Manenoi A, Paull RE (2007) Papaya fruit softening, endoxylanase gene expression, protein and activity. Physiol Plant 131:470–480

    Article  CAS  PubMed  Google Scholar 

  • Morita Y, Saitoh M, Hoshino A, Nitasaka E, Iida S (2006) Isolation of cDNAs for R2R3-MYB, bHLH and WDR transcriptional regulators and identification of c and ca mutations conferring white flowers in the Japanese morning glory. Plant Cell Physiol 47:457–470

    Article  CAS  PubMed  Google Scholar 

  • Norelli JL, Farrell RE Jr, Bassett CL, Baldo AM, Lalli DA, Aldwinckle HS, Wisniewski ME (2009) Rapid transcriptional response of apple to fire blight disease revealed by cDNA suppression subtractive hybridization analysis. Tree Genet Genomes 5:27–40

    Article  Google Scholar 

  • Omer S, Kumar S, Khan BM (2013) Over-expression of a subgroup 4 R2R3 type MYB transcription factor gene from Leucaena leucocephala reduces lignin content in transgenic tobacco. Plant Cell Rep 32:161–171

    Article  CAS  PubMed  Google Scholar 

  • Pang XM, Nada K, Liu JH, Kitashiba H, Honda C, Yamashita H, Tatsuki M, Moriguchi T (2006) Interrelationship between polyamine and ethylene in 1-methylcyclopropene treated apple fruits after harvest. Physiol Plantarum 128:351–359

    Article  CAS  Google Scholar 

  • Rogers LA, Campbell MM (2004) The genetic control of lignin deposition during plant growth and development. New Phytol 164:17–30

    Article  CAS  Google Scholar 

  • Ros Barcelo A (2005) Xylem parenchyma cells deliver the H2O2 necessary for lignification in differentiating xylem vessels. Planta 220:747–756

    Article  CAS  PubMed  Google Scholar 

  • Sonbol FM, Fornale S, Capellades M, Encina A, Tourino S, Torres JL, Rovira P, Ruel K, Puigdomenech P, Rigau J, Caparros-Ruiz D (2009) The maize ZmMYB42 represses the phenylpropanoid pathway and affects the cell wall structure, composition and degradability in Arabidopsis thaliana. Plant Mol Biol 70:283–296

    Article  CAS  PubMed  Google Scholar 

  • Sugar D, Powers KA, Basile SR (2005) Mancozeb and kaolin applications can reduce russet of ‘Comice’ pear. HortTechnology 15(2):272–275

    CAS  Google Scholar 

  • Takahashi T, Kakehi JI (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6

    Article  CAS  PubMed  Google Scholar 

  • Tao ST, Khanizadeh S, Zhang H, Zhang SL (2009) Anatomy, ultrastructure and lignin distribution of stone cells in two Pyrus species. Plant Sci 176:413–419

    Article  CAS  Google Scholar 

  • Van Doorsselaere J, Baucher M, Chognot E, Chabbert B, Tollier MT, Petit-Conil M, Leple JC, Pilate G, Cornu D, Monties B, Montagu MV, Inze D, Boerjan W, Jouanin L (1995) A novel lignin in poplar trees with a reduced caffeic acid/5-hydroxyferulic acid O-methyltransferase activity. Plant J 8:855–864

    Article  Google Scholar 

  • Yoda H, Yamaguchi Y, Sano H (2003) Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in Tobacco plants. Plant Physiol 132:1973–1981

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhou JL, Lee CH, Zhong RQ, Ye ZH (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21:248–266

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu LW, Zhu YD, Jia B, Zhang SM (2009) Study on pear (Pyrus spp.) germplasm resources collected at the protection district of ‘Dangshansuli’ by ISSR markers. Hortic Environ Biotechnol 50:334–340

    CAS  Google Scholar 

Download references

Acknowledgments

This project was supported by the National Natural Science Foundation of China (31101519), the earmarked fund for China Agriculture Research System (CARS-29-14), and the Foundation for Young Talents in universities of Anhui Province (2012SQRL060ZD). The authors thank Prof. Christopher Brian Watkins (Cornell University, NY, USA) for helpful suggestions and paper revises.

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Correspondence to Li-wu Zhu.

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Wei Heng and Li Liu should be regarded as joint first authors.

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Heng, W., Liu, L., Wang, Md. et al. Differentially expressed genes related to the formation of russet fruit skin in a mutant of ‘Dangshansuli’ pear (Pyrus bretchnederi Rehd.) determined by suppression subtractive hybridization. Euphytica 196, 285–297 (2014). https://doi.org/10.1007/s10681-013-1032-x

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  • DOI: https://doi.org/10.1007/s10681-013-1032-x

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