Changes in pericarp morphology, physiology and cell wall composition account for flesh firmness during the ripening of blackberry (Rubus spp.) fruit

Abstract Fruit flesh firmness plays a critical role in controlling blackberry (Rubus spp.) postharvest shelf life. This work aimed to identify the underlying characteristics in pericarp morphology, cell wall hydrolase activity and cell wall composition that account for flesh firmness in soft-fruited ‘Boysen’ and firm-fruited ‘Arapaho’ cultivars that have a similar ripening time of 39 days after flowering (DAF). The fruit firmness of both fruits decreased noticeably at the onset of color change, and this decrease hastened from 33 DAF to ripening despite considerable differences in their temporal changes. The evaluation of pericarp cellular morphology revealed that the disassembly of the cell wall in both fruits was likely initiated at 33 DAF, followed by extreme degradation at 39 DAF. Cell wall hydrolase activity assays indicated that increases in polygalacturonase (PG) and cellulase activity also dramatically occurred in the late softening stages of both fruits. Notably, appreciably higher levels of cellulase, and significant increases in pectin methylesterase (PME), α-L-arabinofuranosidase (α-L-Af) and xyloglucan endotransglycosylase (XET) were only detected in the late ripening stages of ‘Boysen’. In terms of cell wall components, the levels of cell wall material (CWM), cellulose and hemicellulose declined similarly during ripening in both fruits. Comparatively, lower levels of CWM, chelator soluble pectin (CSP), sodium carbonate soluble pectin (SSP), and hemicellulose as well as higher levels of water soluble pectin (WSP) were found in ‘Boysen’ than those in ‘Arapaho’ during maturation and ripening. Overall, the loss of fruit firmness during ripening in blackberry fruit is correlated closely with biochemical changes in cell wall fractions that involve hydrolytic processes, resulting in the breakdown of cell-wall polymers. The low firmness of ‘Boysen’, as determined by cell wall degradation, could be of particular relevance to the function of cell wall degrading enzymes and to the more drastic degradation of cell wall components than that in the firm cv. ‘Arapaho’.

[1]  E. Baldwin,et al.  Ripening Physiology in 'Navaho' Thornless Blackberries: Color, Respiration, Ethylene Production, Softening, and Compositional Changes , 2000 .

[2]  D. Brummell,et al.  Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants , 2001, Plant Molecular Biology.

[3]  R. Sexton,et al.  Cellulase, Fruit Softening and Abscission in Red RaspberryRubus idaeusL. cv Glen Clova , 1997 .

[4]  D. Huber,et al.  Extensive solubilization and depolymerization of cell wall polysaccharides during avocado (Persea americana) ripening involves concerted action of polygalacturonase and pectinmethylesterase , 2000 .

[5]  J. Moore,et al.  'Arapaho' erect, thornless blackberry , 1993 .

[6]  P. Perkins-Veazie,et al.  Cultivar and maturity affect postharvest quality of fruit from erect blackberries , 1996 .

[7]  P. Andrews,et al.  Cell wall hydrolytic enzyme activity during development of nonclimacteric sweet cherry (Prunus avium L.) fruit , 1995 .

[8]  C. Sams,et al.  Changes in cell wall neutral sugar composition during fruit ripening: a species survey , 1984 .

[9]  R. Reeve FRUIT HISTOGENESIS IN RUBUS STRIGOSUS II. ENDOCARP TISSUES , 1954 .

[10]  Mondher Bouzayen,et al.  Ethylene regulation of fruit softening and cell wall disassembly in Charentais melon. , 2007, Journal of experimental botany.

[11]  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.

[12]  R. Tharanathan,et al.  Post-harvest biochemical changes associated with the softening phenomenon in Capsicum annuum fruits , 1996 .

[13]  Paul K. Kintner,et al.  Carbohydrate Interference and Its Correction in Pectin Analysis Using the m‐Hydroxydiphenyl Method , 1982 .

[14]  Cristina M. Oliveira,et al.  Patterns of enzymatic activity of cell wall-modifying enzymes during growth and ripening of apples , 2007 .

[15]  J. Lyons CHILLING INJURY IN PLANTS , 1973 .

[16]  N. Sakurai,et al.  Changes in the cell-wall polysaccharides of outer pericarp tissues of kiwifruit during development. , 2006, Plant physiology and biochemistry : PPB.

[17]  M. Devaux,et al.  Physiological relationships among physical, sensory, and morphological attributes of texture in tomato fruits. , 2007, Journal of experimental botany.

[18]  J. Collins,et al.  Quality of erect-type blackberry fruit after short intervals of controlled atmosphere storage , 2002 .

[19]  A. Bennett,et al.  Modification of Expansin Protein Abundance in Tomato Fruit Alters Softening and Cell Wall Polymer Metabolism during Ripening , 1999, Plant Cell.

[20]  K. Niranjan,et al.  The efficacy of potassium sorbate-coated packaging to control postharvest gray mold in raspberries, blackberries and blueberries , 2016 .

[21]  J. D. Filho,et al.  Conservação pós-colheita de frutos de amoreira-preta , 2003 .

[22]  Hailong Yang,et al.  Changes in fruit firmness, cell wall composition and cell wall degrading enzymes in postharvest blueberries during storage , 2015 .

[23]  S. Fry,et al.  Xyloglucan Endotransglycosylase Activity Increases during Kiwifruit (Actinidia deliciosa) Ripening (Implications for Fruit Softening) , 1993, Plant physiology.

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

[25]  R. Auras,et al.  Comparative shelf life study of blackberry fruit in bio-based and petroleum-based containers under retail storage conditions. , 2011, Food chemistry.

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

[27]  A. Powell,et al.  Cell wall disassembly events in boysenberry (Rubus idaeus L. × Rubus ursinus Cham. & Schldl.) fruit development. , 2007, Functional plant biology : FPB.

[28]  K. Wakabayashi Changes in Cell Wall Polysaccharides During Fruit Ripening , 2000, Journal of Plant Research.

[29]  K. Gross A rapid and sensitive spectrophotometric method for assaying polygalacturonase using 2-cyanoacetamide [Tomato, fruit softening] , 1982 .

[30]  Í. Arozarena,et al.  Andean blackberries (Rubus glaucus Benth) quality as affected by harvest maturity and storage conditions , 2017 .

[31]  L. Howard,et al.  The blackberry fruit: a review on its composition and chemistry, metabolism and bioavailability, and health benefits. , 2012, Journal of agricultural and food chemistry.

[32]  A. Powell,et al.  Temporal sequence of cell wall disassembly events in developing fruits. 2. Analysis of blueberry (Vaccinium species). , 2007, Journal of agricultural and food chemistry.

[33]  R. E. Hardenburg,et al.  The commercial storage of fruits, vegetables, and florist and nursery stocks , 1986 .

[34]  Z. Sulová,et al.  Xyloglucan endotransglycosylase: evidence for the existence of a relatively stable glycosyl-enzyme intermediate. , 1998, The Biochemical journal.

[35]  M. Bourne Food Texture and Viscosity: Concept and Measurement , 2002 .

[36]  R. Sexton,et al.  Fruit abscission and ethylene production of four blackberry cultivars (Rubus spp.) , 1993 .

[37]  J. Labavitch,et al.  Cell wall metabolism during maturation, ripening and senescence of peach fruit. , 2004, Journal of experimental botany.

[38]  Yunfei Li,et al.  Changes in firmness, cell wall composition and cell wall hydrolases of grapes stored in high oxygen atmospheres , 2005 .

[39]  Haiyan Yang,et al.  Effect of drought stress on physiological changes and leaf surface morphology in the blackberry , 2017, Brazilian Journal of Botany.

[40]  M. Quesada,et al.  The polygalacturonase FaPG1 gene plays a key role in strawberry fruit softening. , 2009, Plant signaling & behavior.

[41]  A. Tateishi β-Galactosidase and α-L-Arabinofuranosidase in Cell Wall Modification Related with Fruit Development and Softening , 2008 .

[42]  P. Civello,et al.  Novel insights of ethylene role in strawberry cell wall metabolism. , 2016, Plant science : an international journal of experimental plant biology.

[43]  F. M. Basiouny ETHYLENE EVOLUTION AND QUALITY OF BLACKBERRY FRUIT AS INFLUENCED BY HARVEST TIME AND STORAGE INTERVALS , 1995 .

[44]  D. Mohnen Pectin structure and biosynthesis. , 2008, Current opinion in plant biology.

[45]  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.

[46]  F. Costa,et al.  Texture profiling of blueberries (Vaccinium spp.) during fruit development, ripening and storage , 2013 .

[47]  C. Brady,et al.  Endo-1,4-[beta]-Glucanase, Xyloglucanase, and Xyloglucan Endo-Transglycosylase Activities Versus Potential Substrates in Ripening Tomatoes , 1994, Plant physiology.

[48]  J. Monro,et al.  Changes in elements, pectic substances and organic acids during development of boysenberry fruit , 1987 .

[49]  R. Tharanathan,et al.  Fruit Ripening Phenomena–An Overview , 2007, Critical reviews in food science and nutrition.

[50]  Yunbo Luo,et al.  Modification of hemicellulose polysaccharides during ripening of postharvest banana fruit , 2009 .

[51]  A. Bennett,et al.  Polygalacturonases: many genes in search of a function. , 1998, Plant physiology.

[52]  E. Macrae,et al.  Xyloglucan endotransglycosylase activity during fruit development and ripening of apple and kiwifruit , 1996 .

[53]  F. Lawrence A Review of Interspecific Hybridization in Rubus , 1986, HortScience.

[54]  J. Labavitch,et al.  Cell Wall Metabolism in Ripening Fruit (VI. Effect of the Antisense Polygalacturonase Gene on Cell Wall Changes Accompanying Ripening in Transgenic Tomatoes) , 1993, Plant physiology.

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

[56]  S. Fry,et al.  Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. , 1992, The Biochemical journal.