Review
Cell wall modifications during fruit ripening: when a fruit is not the fruit

https://doi.org/10.1016/j.tifs.2007.07.002Get rights and content

Textural changes that lead to softening of fruits are accompanied by loss of neutral sugars, solubilisation and depolymerisation of the polysaccharides of the cell wall, and rearrangements of their associations, as the result of the combined action of several cell wall-modifying enzymes, acting in both pectic and hemicellulosic fractions. Recent studies on the structure of the plant cell wall have disclosed a large number and type of biochemical linkages between the components. Such linkages are potential targets for enzymatic action and draw attention to the putative involvement of several members of enzymes able to act and modify its structure in a developmental and coordinated way. Extensive work on fruit ripening has been done using tomato (Solanum lycopersicum [Lycopersicon esculentum Mill.]) as a plant model and the information concerning fruits other than model species is fragmented and incomplete. However, recent data from the literature had disclosed that differences exist between fruits, and even between cultivars of the same fruit species. These differences exist in the type and extent of the modification of the polysaccharides of the cell wall and in the expression and regulation of cell wall-modifying enzymes. In addition, genetic manipulation of cell wall-modifying genes re-opened the discussion about the real effect of these enzymes in the cell wall and their role in fruit softening. Moreover, the function of each enzyme has been proposed based on its homology with other annotated sequences, but, in most cases, confirmation of activity in planta and substrate specificity remains to be investigated. This aspect and recognized limitations of the in vitro enzymatic activity assays also need to be considered when discussing their role. This paper provides a critical review on the current knowledge concerning these differences and emphasises the need of using other species and more accurate methodologies to investigate general mechanisms and fruit specificities of softening among different fleshy fruits.

Section snippets

Introduction: the significance of fruit ripening and associated textural modifications

Once regarded as a senescent phenomenon, fruit ripening is now considered as a well coordinated and genetically determined process of tissue differentiation. Events like pigment accumulation and volatile production are included among universal ripening changes but do not occur usually in senescence (Brady, 1987). Fruit ripening is a crucial physiological process for plants, since it represents the terminal stage of development in which the matured seeds are released. Therefore, it is the

Botanical, compositional and developmental differences between fruits

Different fruits differ markedly in their botanical origin, polysaccharide and protein composition, cell wall structure, enzymatic metabolism, growing and ripening pattern, or softening behaviour. These differences that reflect pulp firmness, rate of softening and overall texture are now recognized not only between different species but also between different cultivars, varieties and selections from the same species.

Different fruits have distinct botanical origins. The botanical definition of

Cell wall modifications in structure and composition during fruit ripening

Changes in the structure of the cell wall are associated with dissolution of the middle lamella and disruption of the primary cell wall (Crookes & Grierson, 1983). Structural changes in pectin, hemicellulose and cellulose together are assumed to be responsible for the alteration of cell wall structure during ripening-related loss of firmness (Huber, 1983, Seymour et al., 1990). These changes include not only solubilisation and depolymerisation of the polysaccharides but also rearrangements of

Parallels and differences in the temporal pattern of ripening-related cell wall modifications in distinct fruits

Knowledge about the temporal pattern in which these modifications take place is important to the overall understanding of the whole process. Using “Charentais” melon (C. melo L.), a fruit which softens in a very short period of time, a sequential pattern of polysaccharide modifications was proposed for the first time (Rose et al., 1998). The results obtained suggest that early events in melon fruit softening are associated with the regulated disassembly of a tightly bound fraction of xyloglucan

The expression and activity of cell wall-modifying enzymes

The plant cell wall contains many enzymes able to modify matrix polysaccharides, including several types of endoglycanases ordered to cleave the backbone of matrix hemicelluloses or pectins; glycosidases that may remove side-chains, thus allowing greater interactions between polysaccharide backbones; transglycosylases that may cut hemicelluloses and ligate them together, or esterases and acetylases that can remove methyl or acetyl groups from pectins and cleave ester linkages between

Probing the function of ripening-related cell wall-modifying enzymes using altered genetic backgrounds

Results from genetically modified lines in which fruit ripening-associated cell wall genes have been suppressed or overexpressed and analysis of gene expression in known ripening-impaired mutants, have provided more direct information about the possible function of each gene family and isoform in ripening. This sub-section reviews and discusses the literature concerning the results of the manipulation of individual cell wall-modifying genes in fruits, and its outcome in fruit softening and

Methodological constrains to the study of cell wall-related activities

The role of each enzyme cannot be explained by studying a single specific isoform since the presence of several isoforms, with distinct patterns of expression, may mask the total activity in a given developmental stage. Hence, assays for monitoring the changes in the activity during the development of the fruit are still informative and needed to complement the studies of genetic expression. Examination of the gene expression and enzyme activity data in the literature often shows a poor

Non-enzymatic control of cell wall modifications during ripening

More recently, it was suggested that ripening could occur as the result of non-enzymatic modifications of the cell wall components, both pectins and xyloglucans. Membrane permeabilisation occurring early in ripening, leads to the release of ascorbate into the apoplast, where it may trigger apoplastic hydroxyl production via the Fenton reaction and this radical is potentially involved in non-enzymatic scission of plant cell wall polysaccharides.

During ripening of tomato, excised pieces of living

Taking advantage of natural variation for improving texture in fruits

This review points out important differences concerning the softening behaviour of individual fruits. This aspect means that each fruit cultivar from a given species should be regarded to have putatively some specificities in relation to softening-related cell wall metabolism. This implies that a substantial amount of work must be undertaken in order to clarify specific aspects of fruit softening, in order to fully understand the mechanism. However, these natural occurring differences can be

Conclusions and prospects

Dietary guidelines recommending the consumption of fresh fruits will not be succeeded if consumer dissatisfaction with the product quality limits fruit consumption. However, contemporary traditional postharvest approaches for fruits are not sufficient to meet the increasing consumer's demand on quality due to the development of undesirable characteristics. Increasing the storage life of fruits through the development of new techniques aimed to reduce the rate of deterioration while maintaining

References (283)

  • C.A. Bustamante et al.

    β-xylosidase in strawberry fruit: isolation of a full-length gene and analysis of its expression and enzymatic activity in cultivars with constrasting firmness

    Plant Science

    (2006)
  • D. Dellapenna et al.

    The beta subunit of tomato fruit polygalacturonase isoenzyme 1 defines a new class of plant cell proteins involved in pectin metabolism: AroGPs (Aromatic amino acid rich Glyco Proteins). Pectins and pectinases: proceedings of an international symposium, Wageningen, the Netherlands. Elsevier Science

    Progress in Biotechnology

    (1996)
  • J.M. Denès et al.

    Different action patterns for apple pectin methylesterase at pH 7.0 and 4.5

    Carbohydrate Research

    (2000)
  • M.C. Dotto et al.

    Expression of expansin genes in strawberry varieties with contrasting fruit firmness

    Plant Physiology and Biochemistry

    (2006)
  • B. Fils-Lycaon et al.

    Changes in glycosidase activities during development and ripening of melon

    Postharvest Biology and Technology

    (1991)
  • S. Fonseca et al.

    Monitoring gene expression along pear fruit development, ripening and senescence using cDNA microarrays

    Plant Science

    (2004)
  • C. Frenkel et al.

    Pectin methylesterase regulates methanol and ethanol accumulation in ripening tomato (Lycopersicon esculentum) fruit

    The Journal of Biological Chemistry

    (1998)
  • L.F. Goulao et al.

    Patterns of enzymatic activity of cell wall-modifying enzymes during growth and ripening of apples

    Postharvest Biology and Technology

    (2007)
  • K.C. Gross et al.

    Changes in cell wall neutral sugar composition during fruit ripening: a species survey

    Phytochemistry

    (1984)
  • F.B. Abeles et al.

    Increased cellulase activity during blackberry fruit ripening

    HortScience

    (1989)
  • F. Agius et al.

    Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase

    Nature Biotechnology

    (2003)
  • A. Ahmed et al.

    Cell wall metabolism in ripening fruit. I. Cell wall changes in ripening ‘Bartlett’ pears

    Plant Physiology

    (1980)
  • A. Ahmed et al.

    Cell wall metabolism in ripening fruit. II. Changes in carbohydrate-degrading enzymes in ripening ‘Bartlett’ pears

    Plant Physiology

    (1980)
  • Z.M. Ali et al.

    Isolation, characterization and significance of papaya β-galactanases to cell wall modification and fruit softening during ripening

    Physiologia Plantarum

    (1998)
  • D.P.F. Almeida et al.

    Apoplastic pH and inorganic ion levels in tomato fruit: a potential means for regulation of cell wall metabolism during ripening

    Physiologia Plantarum

    (1999)
  • L. Aravind

    Guilty by association: contextual information in genome analysis

    Genome Research

    (2000)
  • D.A. Arrowsmith et al.

    Characterisation of two tomato fruit-expressed cDNAs encoding xyloglucan endo-transglycosylase

    Plant Molecular Biology

    (1995)
  • R.G. Atkinson et al.

    Apple ACC-oxidase and polygalacturonase: ripening-specific gene expression and promoter analysis in transgenic tomato

    Plant Molecular Biology

    (1998)
  • M. Awad et al.

    Postharvest variation in cellulase, polygalacturonase, and pectinmethylesterase in avocado (Persea americana Mill, cv. Fuerte) fruits in relation to respiration and ethylene production

    Plant Physiology

    (1979)
  • M. Awad et al.

    Avocado pectinmethylesterase activity in relation to temperature, ethylene, and ripening

    Journal of the American Society for Horticultural Science

    (1980)
  • J.K. Babbitt et al.

    Effects of growth-regulators on cellulase, polygalacturonase, respiration, color, and texture of ripening tomatoes

    Journal of the American Society for Horticultural Science

    (1973)
  • C. Batisse et al.

    Pectin changes in ripening cherry fruit

    Journal of Food Science

    (1994)
  • R. Ben-Arie et al.

    Ultrastructural changes in the cell walls of ripening apple and pear fruit

    Plant Physiology

    (1979)
  • A. Benítez-Burraco et al.

    Cloning and characterization of two ripening-related strawberry (Fragaria x ananassa cv. Chandler) pectate lyase genes

    Journal of Experimental Botany

    (2003)
  • C. Bonghi et al.

    Endo-ß-1,4-glucanases are involved in peach fruit growth and ripening, and regulated by ethylene

    Physiologia Plantarum

    (1998)
  • T.J. Bootten et al.

    Solid-state 13C-NMR spectroscopy shows that the xyloglucans in the primary cell walls of mung bean (Vigna radiate L.) occur in different domains: a new model for xyloglucan-cellulose interactions in the cell wall

    Journal of Experimental Botany

    (2004)
  • M.C. Bourne

    Fruit texture – overview of trends and problems

    Journal of Texture Studies

    (1979)
  • V. Bourquin et al.

    Xyloglucan endotransglycosylases have a function during the formation of secondary cell walls of vascular tissues

    Plant Cell

    (2002)
  • C.J. Brady

    The pectinesterase of the pulp of the banana fruit

    Australian Journal of Plant Physiology

    (1976)
  • C.J. Brady

    Fruit ripening

    Annual Review of Plant Physiology

    (1987)
  • C.J. Brady et al.

    Polygalacturonase in tomato fruits and the induction of ripening in Lycopersicon esculentum

    Australian Journal of Plant Physiology

    (1982)
  • D.A. Brummell

    Cell wall disassembly in ripening fruit

    Functional Plant Biology

    (2006)
  • D.A. Brummell et al.

    A membrane-anchored E-type endo-1,4-beta-glucanase is localized on Golgi and plasma membranes of higher plants

    Proceedings of the National Academy of Sciences of the USA

    (1997)
  • D.A. Brummell et al.

    Cell wall metabolism during maturation, ripening and senescence of peach fruit

    Journal of Experimental Botany

    (2004)
  • D.A. Brummell et al.

    Antisense suppression of tomato endo-1,4-β-glucanase Cel2 mRNA accumulation increases the force required to break fruit abscission zones but does not affect fruit softening

    Plant Molecular Biology

    (1999)
  • D.A. Brummell et al.

    Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants

    Plant Molecular Biology

    (2001)
  • D.A. Brummell et al.

    Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening

    Plant Cell

    (1999)
  • D.A. Brummell et al.

    Differential expression of expansin gene family members during growth and ripening of tomato fruit

    Plant Molecular Biology

    (1999)
  • D.A. Brummell et al.

    Effect of antisense suppression of endopolygalacturonase activity on polyuronide molecular weight in ripening tomato fruit and fruit homogenates

    Plant Physiology

    (1997)
  • P. Bucheli et al.

    Definition of biochemical and molecular markers (quality trait loci) for tomato flavour as tools in breeding

    Acta Horticulturae

    (1999)
  • Cited by (402)

    • Ascorbic acid as a master redox regulator of fruit ripening

      2024, Postharvest Biology and Technology
    View all citing articles on Scopus
    View full text