Transcriptome analysis of ripe and unripe fruit tissue of banana identifies major metabolic networks involved in fruit ripening process

详细信息    查看全文

• 作者：Mehar Hasan Asif (1) (2)
  Deepika Lakhwani (1) (2)
  Sumya Pathak (1)
  Parul Gupta (1)
  Sumit K Bag (1) (2)
  Pravendra Nath (1)
  Prabodh Kumar Trivedi (1) (2)
  
  1. CSIR-National Botanical Research Institute ; Council of Scientific and Industrial Research (CSIR-NBRI) ; Rana Pratap Marg ; Lucknow ; 226001 ; India
  2. Academy of Scientific and Innovative Research (AcSIR) ; Anusandhan Bhawan ; 2 Rafi Marg ; New Delhi ; 110 001 ; India
  
• 关键词：Banana ; Ethylene ; Fruit ripening ; Musa acuminata ; Transcriptome
• 刊名：BMC Plant Biology
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：14
• 期：1
• 全文大小：1,408 KB
• 参考文献：1. Bapat, VA, Trivedi, PK, Ghosh, A, Sane, VA, Ganapathi, TR, Nath, P (2010) Ripening of fleshy fruit: molecular insight and the role of ethylene. Biotechnol Adv 28: pp. 94-107 CrossRef
  2. Klee, HJ, Giovannoni, JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45: pp. 41-59 CrossRef
  3. Nath, P, Sane, VA, Sane, AP, Trivedi, PK Regulation of Plant Gene Expression. In: RA, M eds. (2005) Encylopedia of Molecular and Cell Biology and Molecular Medicine. Wiley-VCH Verlag Gmbh & Co, Weinheim, Germany, pp. 307-358
  4. D'Hont, A, Denoeud, F, Aury, JM, Baurens, FC, Carreel, F, Garsmeur, O, Noel, B, Bocs, S, Droc, G, Rouard, M, Silva, C, Jabbari, K, Cardi, C, Poulain, J, Souquet, M, Labadie, K, Jourda, C, Lengell茅, J, Rodier-Goud, M, Alberti, A, Bernard, M, Correa, M, Ayyampalayam, S, Mckain, MR, Leebens-Mack, J, Burgess, D, Freeling, M, Mb茅gui茅-A-Mb茅gui茅, D, Chabannes, M, Wicker, T (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488: pp. 213-217 CrossRef
  5. Droc, G, Larivi猫re, D, Guignon, V, Yahiaoui, N, This, D, Garsmeur, O, Dereeper, A, Hamelin, C, Argout, X, Dufayard, JF, Lengelle, J, Baurens, FC, Cenci, A, Pitollat, B, D'Hont, A, Ruiz, M, Rouard, M, Bocs, S (2013) The banana genome hub. Database (oxford) 2013: pp. bat035 CrossRef
  6. Lohani, S, Trivedi, PK, Nath, P (2004) Changes in activities of cell wall hydrolases during ethylene-induced ripening in banana: effect of 1-MCP, ABA and IAA. Postharvest Biol Technol 31: pp. 119-126 CrossRef
  7. Asif, MH, Nath, P (2005) Expression of multiple forms of polygalacturonase gene during ripening in banana fruit. Plant Physiol Biochem 43: pp. 177-184 CrossRef
  8. Trivedi, PK, Nath, P (2004) MaExp1, an ethylene-induced expansin from ripening banana fruit. Plant Sci 167: pp. 1351-1358 CrossRef
  9. Asha, , Sane, VA, Sane, AP, Nath, P (2007) Multiple forms of 脦卤鈭抏xpansin genes are expressed during banana fruit ripening and development. Postharvest Biol Technol 45: pp. 184-192 CrossRef
  10. Roy Choudhury, S, Roy, S, Singh, SK, Sengupta, DN (2010) Molecular characterization and differential expression of beta-1,3-glucanase during ripening in banana fruit in response to ethylene, auxin, ABA, wounding, cold and light鈥揹ark cycles. Plant Cell Rep 29: pp. 813-828 CrossRef
  11. Kesari, R, Trivedi, PK, Nath, P (2007) Ethylene-induced ripening in banana evokes expression of defense and stress related genes in fruit tissue. Postharvest Biol Technol 46: pp. 136-143 CrossRef
  12. Elitzur, T, Vrebalov, J, Giovannoni, JJ, Goldschmidt, EE, Friedman, H (2010) The regulation of MADS-box gene expression during ripening of banana and their regulatory interaction with ethylene. J Exp Bot 61: pp. 1523-1535 CrossRef
  13. Yan, SC, Chen, JY, Yu, WM, Kuang, JF, Chen, WX, Li, XP, Lu, WJ (2011) Expression of genes associated with ethylene-signalling pathway in harvested banana fruit in response to temperature and 1-MCP treatment. J Sci Food Agric 91: pp. 650-657 CrossRef
  14. Clendennen, SK, May, GD (1997) Differential gene expression in ripening banana fruit. Plant Physiol 115: pp. 463-469 CrossRef
  15. Gupta, SM, Srivastava, S, Sane, AP, Nath, P (2006) Differential expression of genes during banana fruit development, ripening and 1-MCP treatment: Presence of distinct fruit specific, ethylene induced and ethylene repressed expression. Postharvest Biol Technol 42: pp. 16-22 CrossRef
  16. Medina-Suarez, R, Manning, K, Fletcher, J, Aked, J, Bird, CR, Seymour, GB (1997) Gene expression in the pulp of ripening bananas. Two-dimensional sodium dodecyl sulfate-polyacrylamide gel electrophoresis of in vitro translation products and cDNA cloning of 25 different ripening-related mRNAs. Plant Physiol 115: pp. 453-461 CrossRef
  17. Gupta, P, Goel, R, Pathak, S, Srivastava, A, Singh, SP, Sangwan, RS, Asif, MH, Trivedi, PK (2013) De novo assembly, functional annotation and comparative analysis of Withania somnifera leaf and root transcriptomes to identify putative genes involved in the withanolides biosynthesis. PloS One 8: pp. 1932-6203 CrossRef
  18. Pathak, S, Lakhwani, D, Gupta, P, Mishra, , Brij, K, Shukla, S, Asif, MH, Trivedi, PK (2013) Comparative Transcriptome Analysis Using High Papaverine Mutant of Papaver somniferum Reveals Pathway and Uncharacterized Steps of Papaverine Biosynthesis. PloS one 8: pp. e65622 CrossRef
  19. Blanca, J, Esteras, C, Ziarsolo, P, P茅rez, D, Fern茫 Ndez-Pedrosa, V, Collado, C, Rodr茫 Guez de Pablos, R, Ballester, A, Roig, C, Ca帽izares, J, Pic贸, B (2012) Transcriptome sequencing for SNP discovery across Cucumis melo. BMC Genomics 13: pp. 280 CrossRef
  20. Gonzalez-Ibeas, D, Blanca, J, Donaire, L, Saladie, M, Mascarell-Creus, A, Cano-Delgado, A, Garcia-Mas, J, Llave, C, Aranda, MA (2011) Analysis of the melon (Cucumis melo) small RNAome by high-throughput pyrosequencing. BMC Genomics 12: pp. 393 CrossRef
  21. Martinelli, F, Uratsu, SL, Albrecht, U, Reagan, RL, Phu, ML, Britton, M, Buffalo, V, Fass, J, Leicht, E, Zhao, W, Lin, D, D'Souza, R, Davis, CE, Bowman, KD, Dandekar, AM (2012) Transcriptome profiling of citrus fruit response to huanglongbing disease. PLoS One 7: pp. e38039 CrossRef
  22. Yun, Z, Jin, S, Ding, Y, Wang, Z, Gao, H, Pan, Z, Xu, J, Cheng, Y, Deng, X (2012) Comparative transcriptomics and proteomics analysis of citrus fruit, to improve understanding of the effect of low temperature on maintaining fruit quality during lengthy post-harvest storage. J Exp Bot 63: pp. 2873-2893 CrossRef
  23. Rowland, LJ, Alkharouf, N, Darwish, O, Ogden, EL, Polashock, JJ, Bassil, NV, Main, D (2012) Generation and analysis of blueberry transcriptome sequences from leaves, developing fruit, and flower buds from cold acclimation through deacclimation. BMC Plant Biol 12: pp. 46 CrossRef
  24. Gongora-Castillo, E, Fajardo-Jaime, R, Fernandez-Cortes, A, Jofre-Garfias, AE, Lozoya-Gloria, E, Martinez, O, Ochoa-Alejo, N, Rivera-Bustamante, R (2012) The capsicum transcriptome DB: a "hot" tool for genomic research. Bioinformation 8: pp. 43-47 CrossRef
  25. Feng, C, Chen, M, Xu, CJ, Bai, L, Yin, XR, Li, X, Allan, AC, Ferguson, IB, Chen, KS (2012) Transcriptomic analysis of Chinese bayberry (Myrica rubra) fruit development and ripening using RNA-Seq. BMC Genomics 13: pp. 19 CrossRef
  26. Yu, K, Xu, Q, Da, X, Guo, F, Ding, Y, Deng, X (2012) Transcriptome changes during fruit development and ripening of sweet orange (Citrus sinensis). BMC Genomics 13: pp. 10 CrossRef
  27. Richardson, AC, Boldingh, HL, McAtee, PA, Gunaseelan, K, Luo, Z, Atkinson, RG, David, KM, Burdon, JN, Schaffer, RJ (2011) Fruit development of the diploid kiwifruit, Actinidia chinensis 'Hort16A'. BMC Plant Biol 11: pp. 182 CrossRef
  28. Pastore, C, Zenoni, S, Tornielli, GB, Allegro, G, Dal Santo, S, Valentini, G, Intrieri, C, Pezzotti, M, Filippetti, I (2011) Increasing the source/sink ratio in Vitis vinifera (cv Sangiovese) induces extensive transcriptome reprogramming and modifies berry ripening. BMC Genomics 12: pp. 631 CrossRef
  29. Guillaumie, S, Fouquet, R, Kappel, C, Camps, C, Terrier, N, Moncomble, D, Dunlevy, JD, Davies, C, Boss, PK, Delrot, S (2011) Transcriptional analysis of late ripening stages of grapevine berry. BMC Plant Biol 11: pp. 165 CrossRef
  30. Lee, JM, Joung, JG, McQuinn, R, Chung, MY, Fei, Z, Tieman, D, Klee, H, Giovannoni, J (2012) Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation. Plant J 70: pp. 191-204 CrossRef
  31. Guo, S, Liu, J, Zheng, Y, Huang, M, Zhang, H, Gong, G, He, H, Ren, Y, Zhong, S, Fei, Z, Xu, Y (2011) Characterization of transcriptome dynamics during watermelon fruit development: sequencing, assembly, annotation and gene expression profiles. BMC Genomics 12: pp. 454 CrossRef
  32. Romero, P, Lafuente, MT, Rodrigo, MJ (2012) The citrus ABA signalosome: identification and transcriptional regulation during sweet orange fruit ripening and leaf dehydration. J Exp Bot 63: pp. 4931-4945 CrossRef
  33. Kumar, S, Asif, MH, Chakrabarty, D, Tripathi, RD, Trivedi, PK (2011) Differential expression and alternative splicing of rice sulphate transporter family members regulate sulphur status during plant growth, development and stress conditions. Funct Integr Genomics 11: pp. 259-273 CrossRef
  34. Thatcher, SR, Zhou, W, Leonard, A, Wang, BB, Beatty, M, Zastrow-Hayes, G, Zhao, X, Baumgarten, A, Li, B (2014) Genome-wide analysis of alternative splicing in Zea mays: landscape and genetic regulation. Plant Cell 26: pp. 3472-3487 CrossRef
  35. Stekel, DJ, Git, Y, Falciani, F (2000) The comparison of gene expression from multiple cDNA libraries. Genome Res 10: pp. 2055-2061 CrossRef
  36. Brummell, DA, Harpster, MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47: pp. 311-339 CrossRef
  37. Munoz-Bertomeu, J, Miedes, E, Lorences, EP (2013) Expression of xyloglucan endotransglucosylase/hydrolase (XTH) genes and XET activity in ethylene treated apple and tomato fruits. J Plant Physiol 170: pp. 1194-1201 CrossRef
  38. Herrmann, KM (1995) The shikimate pathway: early steps in the biosynthesis of aromatic compounds. Plant Physiol 7: pp. 907-919
  39. Boudhrioua, N, Giampaoli, P, Bonazzi, C (2003) Changes in aromatic components of banana during ripening and air-drying. LWT Food Sci Technol 36: pp. 633-642 CrossRef
  40. Nath, PTP, Sane, VA, Sane, AP Role of ethylene in fruit ripening. In: NA, K eds. (2006) Ethylene Action in Plants. Springer-Verlag, Berlin Heidelberg, pp. 151-176 CrossRef
  41. Hoffmann, L, Maury, S, Martz, F, Geoffroy, P, Legrand, M (2003) Purification, cloning, and properties of an acyltransferase controlling shikimate and quinate ester intermediates in phenylpropanoid metabolism. J Biol Chem 278: pp. 95-103 CrossRef
  42. Beekwilder, J, Alvarez-Huerta, M, Neef, E, Verstappen, FWA, Bouwmeester, HJ, Aharoni, A (2004) Functional characterization of enzymes forming volatile esters from strawberry and banana. Plant Physiol 135: pp. 1865-1878 CrossRef
  43. Asif, MH, Pathak, N, Solomos, T, Trivedi, PK (2009) Effect of low oxygen, temperature and 1-methylcyclopropene on the expression of genes regulating ethylene biosynthesis and perception during ripening in apple. S Afr J Bot 75: pp. 137-144 CrossRef
  44. Asif, MH, Lakhwani, D, Pathak, S, Bhambhani, S, Bag, SK, Trivedi, PK (2013) Genome-wide identification and expression analysis of the mitogen-activated protein kinase gene family from banana suggest involvement of specific members in different stages of fruit ripening. Funct Integr Genomics 14: pp. 161-175 CrossRef
  45. Jin, J, Zhang, H, Kong, L, Gao, G, Luo, J (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42: pp. D1182-D1187 CrossRef
  46. Martel, C, Vrebalov, J, Tafelmeyer, P, Giovannoni, JJ (2011) The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol 157: pp. 1568-1579 CrossRef
  47. Jourda, C, Cardi, C, Mbeguie, AMD, Bocs, S, Garsmeur, O, D'Hont, A, Yahiaoui, N (2014) Expansion of banana (Musa acuminata) gene families involved in ethylene biosynthesis and signalling after lineage-specific whole-genome duplications. New Phytol 202: pp. 986-1000 CrossRef
  48. Asif, M, Dhawan, P, Nath, P (2000) A simple procedure for the isolation of high quality RNA from ripening banana fruit. Plant Mol Biol Rep 18: pp. 109-115 CrossRef
  49. Altschul, SF, Gish, W, Miller, W, Myers, EW, Lipman, DJ (1990) Basic local alignment search tool. J Mol Biol 215: pp. 403-410 CrossRef
  50. Langmead, B, Salzberg, S (2012) Fast gapped-read alignment with Bowtie2. Nat Methods 9: pp. 357-359 CrossRef
  51. Anders, S, Huber, W (2010) Differential expression analysis for sequence count data. Genome Biol 11: pp. R106 CrossRef
  
• 刊物主题：Plant Sciences; Agriculture; Tree Biology;
• 出版者：BioMed Central
• ISSN：1471-2229

文摘

Background Banana is one of the most important crop plants grown in the tropics and sub-tropics. It is a climacteric fruit and undergoes ethylene dependent ripening. Once ripening is initiated, it proceeds at a fast rate making postharvest life short, which can result in heavy economic losses. During the fruit ripening process a number of physiological and biochemical changes take place and thousands of genes from various metabolic pathways are recruited to produce a ripe and edible fruit. To better understand the underlying mechanism of ripening, we undertook a study to evaluate global changes in the transcriptome of the fruit during the ripening process. Results We sequenced the transcriptomes of the unripe and ripe stages of banana (Musa accuminata; Dwarf Cavendish) fruit. The transcriptomes were sequenced using a 454 GSFLX-Titanium platform that resulted in more than 7,00,000 high quality (HQ) reads. The assembly of the reads resulted in 19,410 contigs and 92,823 singletons. A large number of the differentially expressed genes identified were linked to ripening dependent processes including ethylene biosynthesis, perception and signalling, cell wall degradation and production of aromatic volatiles. In the banana fruit transcriptomes, we found transcripts included in 120 pathways described in the KEGG database for rice. The members of the expansin and xyloglucan transglycosylase/hydrolase (XTH) gene families were highly up-regulated during ripening, which suggests that they might play important roles in the softening of the fruit. Several genes involved in the synthesis of aromatic volatiles and members of transcription factor families previously reported to be involved in ripening were also identified. Conclusions A large number of differentially regulated genes were identified during banana fruit ripening. Many of these are associated with cell wall degradation and synthesis of aromatic volatiles. A large number of differentially expressed genes did not align with any of the databases and might be novel genes in banana. These genes can be good candidates for future studies to establish their role in banana fruit ripening. The datasets developed in this study will help in developing strategies to manipulate banana fruit ripening and reduce post harvest losses.