Expression patterns of cell wall-modifying genes from banana during fruit ripening and in relationship with finger drop

Few molecular studies have been devoted to the finger drop process that occurs during banana fruit ripening. Recent studies revealed the involvement of changes in the properties of cell wall polysaccharides in the pedicel rupture area. In this study, the expression of cell-wall modifying genes was monitored in peel tissue during post-harvest ripening of Cavendish banana fruit, at median area (control zone) and compared with that in the pedicel rupture area (drop zone). To this end, three pectin methylesterase (PME) and seven xyloglucan endotransglycosylase/hydrolase (XTH) genes were isolated. The accumulation of their mRNAs and those of polygalaturonase, expansin, and pectate lyase genes already isolated from banana were examined. During post-harvest ripening, transcripts of all genes were detected in both zones, but accumulated differentially. MaPME1, MaPG1, and MaXTH4 mRNA levels did not change in either zone. Levels of MaPME3 and MaPG3 mRNAs increased greatly only in the control zone and at the late ripening stages. For other genes, the main molecular changes occurred 1–4 d after ripening induction. MaPME2, MaPEL1, MaPEL2, MaPG4, MaXTH6, MaXTH8, MaXTH9, MaEXP1, MaEXP4, and MaEXP5 accumulated highly in the drop zone, contrary to MaXTH3 and MaXTH5, and MaEXP2 throughout ripening. For MaPG2, MaXET1, and MaXET2 genes, high accumulation in the drop zone was transient. The transcriptional data obtained from all genes examined suggested that finger drop and peel softening involved similar mechanisms. These findings also led to the proposal of a sequence of molecular events leading to finger drop and to suggest some candidates.

[1]  J. Labavitch,et al.  Ethylene and ripening-regulated expression and function of fruit cell wall modifying proteins , 2008 .

[2]  É. Malézieux,et al.  Pre-harvest growth and development, measured as accumulated degree days, determine the post-harvest green life of banana fruit , 2008 .

[3]  M. Asif,et al.  Expression of multiple forms of polygalacturonase gene during ripening in banana fruit. , 2005, Plant physiology and biochemistry : PPB.

[4]  E. Mitcham,et al.  Ripening and cell wall synthesis in normal and mutant tomato fruit , 1991 .

[5]  Roderic D. M. Page,et al.  TreeView: an application to display phylogenetic trees on personal computers , 1996, Comput. Appl. Biosci..

[6]  K. Nishitani,et al.  The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. , 2002, Plant & cell physiology.

[7]  A. Bennett,et al.  ROLE OF CELL WALL HYDROLASES IN FRUIT RIPENING , 1991 .

[8]  B. Fils-Lycaon,et al.  EIN3-like gene expression during fruit ripening of Cavendish banana (Musa acuminata cv. Grande naine). , 2008, Physiologia plantarum.

[9]  A. P. Sane,et al.  Multiple forms of α-expansin genes are expressed during banana fruit ripening and development , 2007 .

[10]  S. Fry Primary cell wall metabolism: tracking the careers of wall polymers in living plant cells. , 2004, The New phytologist.

[11]  S. Ketsa,et al.  Effects of relative humidity on banana fruit drop , 2007 .

[12]  Kathleen Marchal,et al.  PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences , 2002, Nucleic Acids Res..

[13]  K. Nishitani The role of endoxyloglucan transferase in the organization of plant cell walls. , 1997, International review of cytology.

[14]  P. Trivedi,et al.  Changes in activities of cell wall hydrolases during ethylene-induced ripening in banana: effect of 1-MCP, ABA, and IAA , 2004 .

[15]  E. Mellerowicz,et al.  New insights into pectin methylesterase structure and function. , 2007, Trends in plant science.

[16]  L. Camardella,et al.  Pectin methylesterase inhibitor. , 2004, Biochimica et biophysica acta.

[17]  J. Dumville,et al.  Solubilisation of tomato fruit pectins by ascorbate: a possible non-enzymic mechanism of fruit softening , 2003, Planta.

[18]  M. Frohman RACE: rapid amplification of cDNA ends , 1990 .

[19]  Š. Janeček,et al.  Pectin methylesterases: sequence-structural features and phylogenetic relationships. , 2004, Carbohydrate research.

[20]  J. Marriott,et al.  Factors affecting the development of ‘finger drop’ in bananas after ripening , 2007 .

[21]  C. K. Ong,et al.  Isolation and expression of two pectate lyase genes during fruit ripening of banana (Musa acuminata) , 2001 .

[22]  J. Labavitch,et al.  Cell Wall Metabolism in Ripening Fruit (IX. Synthesis of Pectic and Hemicellulosic Cell Wall Polymers in the Outer Pericarp of Mature Green Tomatoes (cv XMT-22) , 1997, Plant physiology.

[23]  J. Rose,et al.  Characterization of a new xyloglucan endotransglucosylase/hydrolase (XTH) from ripening tomato fruit and implications for the diverse modes of enzymic action. , 2006, The Plant journal : for cell and molecular biology.

[24]  S. Brunak,et al.  Improved prediction of signal peptides: SignalP 3.0. , 2004, Journal of molecular biology.

[25]  J. Labavitch,et al.  The linkage between cell wall metabolism and fruit softening: looking to the future , 2007 .

[26]  A. Galston Plant Physiology , 1967, Nature.

[27]  T. Wilkins,et al.  A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). , 1994, Analytical biochemistry.

[28]  Yoshihiro Ugawa,et al.  Plant cis-acting regulatory DNA elements (PLACE) database: 1999 , 1999, Nucleic Acids Res..

[29]  P. Campbell,et al.  Xyloglucan endotransglycosylases: diversity of genes, enzymes and potential wall-modifying functions. , 1999, Trends in plant science.

[30]  K. Nishitani,et al.  A Surprising Diversity and Abundance of Xyloglucan Endotransglucosylase/Hydrolases in Rice. Classification and Expression Analysis1 , 2004, Plant Physiology.

[31]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[32]  Thomas L. Madden,et al.  BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. , 1999, FEMS microbiology letters.

[33]  P. Trivedi,et al.  MaExp1, an ethylene-induced expansin from ripening banana fruit , 2004 .

[34]  H. Eklund,et al.  Crystal structure of plant pectin methylesterase , 2002, FEBS letters.

[35]  J. Meyer,et al.  Recherche d'une loi d'action de la température sur la croissance des fruits du bananier , 1975 .

[36]  D. Brummell Cell wall disassembly in ripening fruit. , 2006, Functional plant biology : FPB.

[37]  E. Mitcham,et al.  Tomato Fruit Cell Wall Synthesis during Development and Senescence : In Vivo Radiolabeling of Wall Fractions Using [C]Sucrose. , 1989, Plant physiology.

[38]  J. Labavitch,et al.  Cell Wall Metabolism in Ripening Fruit : V. Analysis of Cell Wall Synthesis in Ripening Tomato Pericarp Tissue Using a d-[U-C]Glucose Tracer and Gas Chromatography-Mass Spectrometry. , 1991, Plant physiology.

[39]  N. Pathak,et al.  Purification and characterization of polygalacturonase from banana fruit. , 2000, Phytochemistry.

[40]  F. Micheli Pectin methylesterases: cell wall enzymes with important roles in plant physiology. , 2001, Trends in plant science.

[41]  S. Prat,et al.  A cDNA Clone Highly Expressed in Ripe Banana Fruit Shows Homology to Pectate Lyases , 1997, Plant physiology.

[43]  G. Seymour,et al.  Pectate lyase gene expression and enzyme activity in ripening banana fruit , 2003, Plant Molecular Biology.

[44]  J. Labavitch,et al.  Cell Wall Metabolism in Ripening Fruit: IV. Characterization of the Pectic Polysaccharides Solubilized during Softening of ;Bartlett' Pear Fruit. , 1989, Plant physiology.

[45]  R. Newman,et al.  Cell wall changes in ripening kiwifruit: 13C solid state NMR characterisation of relatively rigid cell wall polymers , 2002 .

[46]  R. Paull Ethylene, storage and ripening temperatures affect Dwarf Brazilian banana finger drop , 1996 .

[47]  Thomas Schiex,et al.  Genome Annotation in Plants and Fungi: EuGene as a Model Platform , 2008 .

[48]  S Rozen,et al.  Primer3 on the WWW for general users and for biologist programmers. , 2000, Methods in molecular biology.

[49]  A. Semple,et al.  Influence of the ripening environment on the development of finger drop in bananas , 1989 .

[50]  S. Ketsa,et al.  Physiological and biochemical changes during banana ripening and finger drop , 2006 .

[51]  Dan S. Prestridge,et al.  SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements , 1991, Comput. Appl. Biosci..

[52]  B. Fils-Lycaon,et al.  Extraction and purification of total RNA from banana tissues (small scale). , 2008 .

[53]  Cristina M. Oliveira,et al.  Cell wall modifications during fruit ripening: when a fruit is not the fruit , 2008 .

[54]  J. Labavitch,et al.  Cell Wall Metabolism in Ripening Fruit: I. CELL WALL CHANGES IN RIPENING ;BARTLETT' PEARS. , 1980, Plant physiology.

[55]  A. Bennett,et al.  Cooperative disassembly of the cellulose-xyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. , 1999, Trends in plant science.

[56]  N. Pathak,et al.  Multiple forms of polygalacturonase from banana fruits. , 1998, Phytochemistry.