Analysis of papaya cell wall-related genes during fruit ripening indicates a central role of polygalacturonases during pulp softening

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Fabi, João Paulo ^a   Broetto, Sabrina Garcia ^a   Da Silva, Sarah Lígia Garcia Leme ^a   Zhong, Silin ^b   Lajolo, Franco Maria ^a   Do Nascimento, João Roberto Oliveira ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

POLYGALACTURONASE; RECOMBINANT PROTEIN; VEGETABLE PROTEIN;

ARTICLE; CELL METABOLISM; CELL STRUCTURE; CELL WALL; ENZYME ACTIVITY; FRUIT RIPENING; GENE EXPRESSION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC CORRELATION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PAPAYA; PG1 GENE; PG2 GENE; PG3 GENE; PLANT GENE; PLANT GENETICS; PLANT LEAF; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; ARABIDOPSIS; CARICA; ENZYMOLOGY; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; KINETICS; METABOLISM;

ARABIDOPSIS; CARICA; CELL WALL; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; KINETICS; PLANT LEAVES; PLANT PROTEINS; POLYGALACTURONASE; RECOMBINANT PROTEINS;

EID: 84923258650     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0105685     Document Type: Article

References (47)

1. Fabi JP, Cordenunsi BR, Barreto GPM, Mercadante AZ, Lajolo FM, et al. (2007) Papaya fruit ripening: response to ethylene and 1-methylcyclopropene (1-MCP). J Agric Food Chem 55: 6118-6123. (Pubitemid 47235667)
2. Gapper NE, McQuinn RP, Giovannoni JJ (2013) Molecular and genetic regulation of fruit ripening. Plant Mol Biol 82(6): 575-91.
3. Brummell DA (2006) Cell wall disassembly in ripening fruit. Funct Plant Biol 33: 103-119.
4. Hyodo H, Terao A, Furukawa J, Sakamoto N, Yurimoto H, et al. (2013) Tissue Specific Localization of Pectin-Ca(2+) Cross-Linkages and Pectin Methyl-Esterification during Fruit Ripening in Tomato (Solanum lycopersicum). PLoS One 13; 8(11): e78949.
5. Shiga TM, Fabi JP, Nascimento JRO, Petkowicz CLO, Vriesmann LC, et al. (2009) Changes in cell wall composition associated to the softening of ripening papaya: evidence of extensive solubilisation of large molecular mass galactouronides. J Agric Food Chem 57: 7064-7071.
6. Fabi JP, Cordenunsi BR, Seymour GB, Lajolo FM, Nascimento JRO (2009) Molecular cloning and characterization of a ripening-induced polygalacturonase related to papaya fruit softening. Plant Physiol Biochem 47: 1075-1081.
7. Othman R, Choo TS, Ali ZM, Zainal Z, Lazan H (1998) A full-length beta-galactosidase cDNA sequence from ripening papaya. Plant Physiol 118: 1102-1102.
8. Manenoi A, Paull RE (2007) Papaya fruit softening, endoxylanase gene expression, protein and activity. Physiol Plant 131: 470-480. (Pubitemid 47508547)
9. Jamet E, Roujol D, San-Clement H, Irshad M, Soubigou-Taconnat L, et al. (2009) Cell wall biogenesis of Arabidopsis thaliana elongating cells: transcriptomics complements proteomics. BMC Gen 10: 505.
10. Fabi JP, Seymour GB, Graham NS, Broadley MR, May ST, et al. (2012) Analysis of Ripening-related Gene Expression in Papaya using an Arabidopsis-based Microarray. BMC Plant Biol 12: 242.
11. Fabi JP, Lajolo FM, Nascimento JRO (2009) Cloning and characterization of transcripts differentially expressed in the pulp of ripening papaya. Sci Hort 121: 159-165.
12. Fabi JP, Mendes LRBC, Lajolo FM, Nascimento JRO (2010) Transcript profiling of papaya fruit reveals differentially expressed genes associated with fruit ripening. Plant Sci 179: 225-233.
13. Chen CC, Fu SF, Lee YI, Lin CY, Lin WC, et al. (2012) Transcriptome analysis of age-related gain of callus-forming capacity in Arabidopsis hypocotyls. Plant Cell Physiol 53(8): 1457-69.
14. Santiago-Doménech N, Jiménez-Bermúdez S, Matas AJ, Rose JKC, Muñoz-Blanco J, et al. (2008) Antisense inhibition of a pectate lyase gene supports a role for pectin depolymerization in strawberry fruit softening. J Exp Bot 59: 2769-2779. (Pubitemid 351957501)
15. Quesada MA, Blanco-Portales R, Posé S, García-Gago JA, Jiménez-Bermúdez S, et al. (2009) Antisense down-regulation of the FaPG1 gene reveals an unexpected central role for polygalacturonase in strawberry fruit softening. Plant Physiol 150: 1022-1032.
16. Soh CP, Ali ZM, Lazan H (2006) Characterisation of an alpha-galactosidase with potential relevance to ripening related texture changes. Phytochem 67: 242-254. (Pubitemid 43061352)
17. Lazan H, Ng SY, Goh LY, Ali ZM (2004) Papaya beta-galactosidase/ galactanase isoforms in differential cell wall hydrolysis and fruit softening during ripening. Plant Physiol Biochem 42: 847-853. (Pubitemid 40191566)
18. Mandaokar A, Thines B, Shin B, Lange BM, Choi G, et al. (2006) Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant J 46(6): 984-1008.
19. Bassel GW, Fung P, Chow TF, Foong JA, Provart NJ, et al. (2008) Elucidating the germination transcriptional program using small molecules. Plant Physiol 147(1): 143-55. (Pubitemid 352844349)
20. Yadav RK, Girke T, Pasala S, Xie M, Reddy GV (2009) Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc Natl Acad Sci U S A 106(12): 4941-4946.
21. Dalchau N, Hubbard KE, Robertson FC, Hotta CT, Briggs HM, et al. (2009) Correct biological timing in Arabidopsis requires multiple light-signaling pathways. Proc Natl Acad Sci U S A 107(29): 13171-13176.
22. Ng S, Giraud E, Duncan O, Law SR, Wang Y, et al. (2013) Cyclin-dependent kinase E1 (CDKE1) provides a cellular switch in plants between growth and stress responses. J Biol Chem 288(5): 3449-3459.
23. Sañudo-Barajas JA, Labavitch J, Greve C, Osuna-Enciso T, Muy-Rangel D, et al. (2009) Cell wall disassembly during papaya softening: Role of ethylene in changes in composition, pectin derived oligomers (PDOs) production and wall hydrolases. Postharvest Biol Technol 51: 158-167.
24. Atkinson RG, Sutherland P, Johnston SL, Gunaseelan K, Hallett IC, et al. (2012) Down-regulation of POLYGALACTURONASE1 alters firmness, tensile strength and water loss in apple (Malus x domestica) fruit. BMC Plant Biol 12: 129.
25. Zuber H, Davidian JC, Aubert G, Aimé D, Belghazi M, et al. (2010) The seed composition of Arabidopsis mutants for the group 3 sulfate transporters indicates a role in sulfate translocation within developing seeds. Plant Physiol 154(2): 913-926.
26. Cantu D, Vicente AR, Greve LC, Dewey FM, Bennett AB, et al. (2008) The intersection between cell wall disassembly, ripening, and fruit susceptibility to Botrytis cinerea. Proc Natl Acad Sci U S A 105(3): 859-864. (Pubitemid 351282045)
27. Hiwasa K, Kinugasa Y, Amano S, Hashimoto A, Nakano R, et al. (2003) Ethylene is required for both the initiation and progression of softening in pear (Pyrus communis L.) fruit. J Exp Bot 54: 771-779. (Pubitemid 36189222)
28. Morgutti S, Negrini N, Nocito FF, Ghiani A, Bassi D, et al. (2006) Changes in endopolygalacturonase levels and characterization of a putative endo-PG gene during fruit softening in peach genotypes with nonmelting and melting flesh fruit phenotypes. New Phyt 171: 315-328.
29. Sekine D, Munemura I, Gao M, Mitsuhashi W, Toyomasu T, et al. (2006) Cloning of cDNAs encoding cell-wall hydrolases from pear (Pyrus communis) fruit and their involvement in fruit softening and development of melting texture. Physiol Plant 126: 163-174.
30. Atkinson RG, Schroder R, Hallett IC, Cohen D, MacRae EA (2002). Overexpression of polygalacturonase in transgenic apple trees leads to a range of novel phenotypes involving changes in cell adhesion. Plant Physiol 129: 122-133. (Pubitemid 34527314)
31. Boudart G, Charpentier M, Lafitte C, Martinez Y, Jauneau A, et al. (2003) Elicitor activity of a fungal endopolygalacturonase in tobacco requires a functional catalytic site and cell wall localization. Plant Physiol 131(1): 93-101. (Pubitemid 36141210)
32. Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, et al. (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus) Nature 452: 991-997.
33. Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016.
34. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Bio 340: 783-795. (Pubitemid 38829638)
35. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, et al. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55(4): 611-622.
36. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29 (9): 2002-2007.
37. Thompson JD, Higgis DG, Gibson TJ (1994) CLUSTALW: 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. (Pubitemid 24354800)
38. Langfelder P, Horvath S (2008) WGCNA: An R package for weighted correlation network analysis. BMC Bio 9: 559.
39. Zhang B, Horvath S (2005) A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol 4: 17.
40. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11): 2498-2504. (Pubitemid 37428274)
41. Hames BD, Rickwood D (1990) Gel electrophoresis of proteins - A practical approach. 2nd ed. IRL Press, Oxford University Press. 372p.
42. Nogueira SB, Labate CA, Gozzo FC, Pilau EJ, Lajolo FM, et al. (2012) Proteomic analysis of papaya fruit ripening using 2DE-DIGE. J Proteomics 75(4): 1428-1439.
43. Nascimento JRO, Cordenunsi BR, Lajolo FM (1997) Purification and partial characterization of sucrose-phosphate synthase from pre-climacteric and climacteric bananas (Musa acuminata). J Agri Food Chem 45: 1103-1107. (Pubitemid 127476875)
44. Carpentier SC, Witters E, Laukens K, Deckers P, Swennen R, et al. (2005) Preparation of protein extracts from recalcitrant plant tissues: an evaluation of different methods for two-dimensional gel electrophoresis analysis. Proteomics, 5: 2497-2507. (Pubitemid 40966477)
45. Zhong S, Lin Z, Fray RG, Grierson D (2008) Improved plant transformation vectors for fluorescent protein tagging. Transgenic Res 17(5): 985-989.
46. Spolaore S, Trainotti L, Casadoro G (2001) A simple protocol for transient gene expression in ripe fleshy fruit mediated by Agrobacterium. J Exp Bot 52(357): 845-850. (Pubitemid 32623727)
47. Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33(5): 949-956. (Pubitemid 36339384)