Disassembly of the fruit cell wall by the ripening-associated polygalacturonase and expansin influences tomato cracking

Fangling Jiang , Alfonso Lopez , Shinjae Jeon , Sergio Tonetto de Freitas , Qinghui Yu , Zhen Wu , John M. Labavitch , Shengke Tian , Ann L. T. Powell , Elizabeth Mitcham

Horticulture Research ›› 2019, Vol. 6 ›› Issue (1) : 17

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Horticulture Research ›› 2019, Vol. 6 ›› Issue (1) :17 DOI: 10.1038/s41438-018-0105-3
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Disassembly of the fruit cell wall by the ripening-associated polygalacturonase and expansin influences tomato cracking
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Abstract

Fruit cracking is an important problem in horticultural crop production. Polygalacturonase (SlPG) and expansin (SlEXP1) proteins cooperatively disassemble the polysaccharide network of tomato fruit cell walls during ripening and thereby, enable softening. A Golden 2-like (GLK2) transcription factor, SlGLK2 regulates unripe fruit chloroplast development and results in elevated soluble solids and carotenoids in ripe fruit. To determine whether SlPG, SlEXP1, or SlGLK2 influence the rate of tomato fruit cracking, the incidence of fruit epidermal cracking was compared between wild-type, Ailsa Craig (WT) and fruit with suppressed SlPG and SlEXP1 expression (pg/exp) or expressing a truncated nonfunctional Slglk2 (glk2). Treating plants with exogenous ABA increases xylemic flow into fruit. Our results showed that ABA treatment of tomato plants greatly increased cracking of fruit from WT and glk2 mutant, but not from pg/exp genotypes. The pg/exp fruit were firmer, had higher total soluble solids, denser cell walls and thicker cuticles than fruit of the other genotypes. Fruit from the ABA treated pg/exp fruit had cell walls with less water-soluble and more ionically and covalently-bound pectins than fruit from the other lines, demonstrating that ripening-related disassembly of the fruit cell wall, but not elimination of SlGLK2, influences cracking. Cracking incidence was significantly correlated with cell wall and wax thickness, and the content of cell wall protopectin and cellulose, but not with Ca2+ content.

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Fangling Jiang, Alfonso Lopez, Shinjae Jeon, Sergio Tonetto de Freitas, Qinghui Yu, Zhen Wu, John M. Labavitch, Shengke Tian, Ann L. T. Powell, Elizabeth Mitcham. Disassembly of the fruit cell wall by the ripening-associated polygalacturonase and expansin influences tomato cracking. Horticulture Research, 2019, 6 (1) : 17 DOI:10.1038/s41438-018-0105-3

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References

[1]

Khadivi-Khub, A. Physiological and genetic factors influencing fruit cracking. Acta Physiol. Plant 37, https://doi.org/10.1007/s11738-014-1718-2 (2014).

[2]

Peet, M. M. Fruit cracking in tomato. HortTechnology 2, 216-223 (1992).

[3]

Balbontin, C. et al. Cracking in sweet cherries: a comprehensive review from a physiological, molecular, and genomic perspective. Chil. J. Agr. Res 73, 66-72 (2013).

[4]

Hahn, F. Fuzzy controller decreases tomato cracking in greenhouses. Comput. Electron Agr. 77, 21-27 (2011).

[5]

Khanal, B. P., Grimm, E. & Knoche, M. Fruit growth, cuticle deposition, water uptake, and fruit cracking in jostaberry, gooseberry, and black currant. Sci. Hortic. Amst. 128, 289-296 (2011).

[6]

Huang, X. M. et al. Spraying calcium is not an effective way to increase structural calcium in litchi pericarp. Sci. Hortic. Amst. 117, 39-44 (2008).

[7]

Zoffoli, J. P., Latorre, B. A. & Naranjo, P. Hairline, a postharvest cracking disorder in table grapes induced by sulfur dioxide. Postharvest Biol. Technol. 47, 90-97 (2008).

[8]

Thompson, D. S. Extensiometric determination of the rheological properties of the epidermis of growing tomato fruit. J. Exp. Bot. 52, 1291-1301 (2001).

[9]

Wiedemann, P. & Neinhuis, C. Biomechanics of isolated plant cuticles. Plant Biol. 111, 28-34 (1998).

[10]

Sekse, L. Fruit cracking in sweet cherries (Prunus-Avium L) - some physiological aspects - a mini review. Sci. Hortic. Amst. 63, 135-141 (1995).

[11]

Bargel, H. & Neinhuis, C. Tomato (Lycopersicon esculentum Mill.) fruit growth and ripening as related to the biomechanical properties of fruit skin and isolated cuticle. J. Exp. Bot. 56, 1049-1060 (2005).

[12]

Matas, A. J., Cobb, E. D., Paolillo, D. J. & Niklas, K. J. Crack resistance in cherry tomato fruit correlates with cuticular membrane thickness. Hortscience 39, 1354-1358 (2004).

[13]

Emmons, C. L. W. & Scott, J. W. Environmental and physiological effects on cuticle cracking in tomato. J. Am. Soc. Hortic. Sci. 122, 797-801 (1997).

[14]

Emmons, C. L. W. & Scott, J. W. Ultrastructural and anatomical factors associated with resistance to cuticle cracking in tomato (Lycopersicon esculentum Mill.). Int J. Plant Sci. 159, 14-22 (1998).

[15]

Moctezuma, E., Smith, D. L. & Gross, K. C. Antisense suppression of a beta-galactosidase gene (TBG6) in tomato increases fruit cracking. J. Exp. Bot. 54, 2025-2033 (2003).

[16]

Cao, Y., Tang, X. F., Giovannoni, J., Xiao, F. M. & Liu, Y. S. Functional characterization of a tomato COBRA-like gene functioning in fruit development and ripening. BMC Plant Biol. 12, Artn 211 10.1186/1471-2229-12-211 (2012).

[17]

Ackley, W. B. & Krueger, W. H. Overhead irrigation water quality and the cracking of sweet cherries. HortScience 15, 289-290 (1980).

[18]

Dominguez, E. et al. Tomato fruit continues growing while ripening, affecting cuticle properties and cracking. Physiol. Plant. 146, 473-486 (2012).

[19]

Michailidis, M. et al. Metabolomic and physico-chemical approach unravel dynamic regulation of calcium in sweet cherry fruit physiology. Plant Physiol. Biochem 116, 68-79 (2017).

[20]

Belge, B., Goulao, L. F., Comabella, E., Graell, J. & Lara, I. Refrigerated storage and calcium dips of ripe 'Celeste' sweet cherry fruit: combined effects on cell wall metabolism. Sci. Hortic. Amst. 219, 182-190 (2017).

[21]

Knoche, M. & Peschel, S. Gibberellins increase cuticle deposition in developing tomato fruit. Plant Growth Regul. 51, 1-10 (2007).

[22]

Byers, R. E., Carbaugh, D. H. & Presley, C. N. Stayman fruit cracking as affected by surfactants, plant-growth regulators, and other chemicals. J. Am. Soc. Hortic. Sci. 115, 405-411 (1990).

[23]

de Freitas, S. T., Shackel, K. A. & Mitcham, E. J. Abscisic acid triggers whole-plant and fruit-specific mechanisms to increase fruit calcium uptake and prevent blossom end rot development in tomato fruit. J. Exp. Bot. 62, 2645-2656 (2011).

[24]

Koyama, K., Sadamatsu, K. & Goto-Yamamoto, N. Abscisic acid stimulated ripening and gene expression in berry skins of the Cabernet Sauvignon grape. Funct. Integr. Genom. 10, 367-381 (2010).

[25]

Powell, A. L. T. et al. Uniform ripening encodes a golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336, 1711-1715 (2012).

[26]

Nguyen, C. V. et al. Tomato GOLDEN2-LIKE transcription factors reveal molecular gradients that function during fruit development and ripening. Plant Cell 26, 585-601 (2014).

[27]

Powell, A. L. T., Kalamaki, M. S., Kurien, P. A., Gurrieri, S. & Bennett, A. B. Simultaneous transgenic suppression of LePG and LeExp1 influences fruit texture and juice viscosity in a fresh market tomato variety. J. Agric. Food Chem. 51, 7450-7455 (2003).

[28]

Vicente, A. R., Powell, A., Greve, L. C. & Labavitch, J. M. Cell wall disassembly events in boysenberry (Rubus idaeus L. x Rubus ursinus Cham. & Schldl.) fruit development. Funct. Plant Biol. 34, 614-623 (2007).

[29]

Akpinar-bayizit, A., Turan, M. A., Yilmaz-ersan, L. & Taban, N. Inductively coupled plasma optical-emission spectroscopy determination of major and minor elements in vinegar. Not. Bot. Hort. Agrobot. Cluj. 38, 64-68 (2010).

[30]

Mollet, J. C., Park, S. Y., Nothnagel, E. A. & Lord, E. M. A lily stylar pectin is necessary for pollen tube adhesion to an in vitro stylar matrix. Plant Cell 12, 1737-1749 (2000).

[31]

Sun, Q., Greve, L. C. & Labavitch, J. M. Polysaccharide compositions of intervessel pit membranes contribute to Pierce's disease resistance of grapevines. Plant Physiol. 155, 1976-1987 (2011).

[32]

Zhang, Q. et al. Phosphatidic acid regulates microtubule organization by interacting with MAP65-1 in response to salt stress in Arabidopsis. Plant Cell 24, 4555-4576 (2012).

[33]

Knox, J. P. The use of antibodies to study the architecture and developmental regulation of plant cell walls. Int. Rev. Cytol. 171, 79-120 (1997).

[34]

Schuch, W. et al. Fruit-quality characteristics of transgenic tomato fruit with altered polygalacturonase activity. Hortscience 26, 1517-1520 (1991).

[35]

Kramer, M. et al. Postharvest evaluation of transgenic tomatoes with reduced levels of polygalacturonase: processing, firmness and disease resistance. Postharvest Biol. Technol. 1, 241-255 (1992).

[36]

Capel, C. et al. Multi-environment QTL mapping reveals genetic architecture of fruit cracking in a tomato RIL Solanum lycopersicum x S-pimpinellifolium population. Theor. Appl. Genet 130, 213-222 (2017).

[37]

Kasai, S., Hayama, H., Kashimura, Y., Kudo, S. & Osanai, Y. Relationship between fruit cracking and expression of the expansin gene MdEXPA3 in ‘Fuji’ apples (Malus domestica Borkh.). Sci. Hortic. Amst. 116, 194-198 (2008).

[38]

Brummell, D. A. et al. Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell 11, 2203-2216 (1999).

[39]

Huang, X. M. et al. Cell wall modifications in the pericarp of litchi (Litchi chinensis Sonn.) cultivars that differ in their resistance to cracking. J. Hortic. Sci. Biotechnol. 81, 231-237 (2006).

[40]

Yong, W., Lu, W. J., Li, J. G. & Jiang, Y. M. Differential expression of two expansin genes in developing fruit of cracking-susceptible and -resistant litchi cultivars. J. Am. Soc. Hortic. Sci. 131, 118-121 (2006).

[41]

Marondedze, C., Gehring, C. & Thomas, L. Dynamic changes in the date palm fruit proteome during development and ripening. Hortic. Res. 1, 14039 (2014).

[42]

Shi, Y., Jiang, L., Zhang, L., Kang, R. & Yu, Z. Dynamic changes in proteins during apple (Malus x domestica) fruit ripening and storage. Hortic. Res. 1, 6 (2014).

[43]

Somerville, C. et al. Toward a systems approach to understanding plant-cell walls. Science 306, 2206-2211 (2004).

[44]

Dellapenna, D., Alexander, D. C. & Bennett, A. B. Molecular-cloning of tomato fruit polygalacturonase-analysis of polygalacturonase messenger-rna levels during ripening. Proc. Natl Acad. Sci. USA 83, 6420-6424 (1986).

[45]

Gross, K. C. & Wallner, S. J. Degradation of cell wall polysaccharides during tomato fruit ripening. Plant Physiol. 63, 117-120 (1979).

[46]

Cantu, D. et al. The intersection between cell wall disassembly, ripening, and fruit susceptibility to Botrytis cinerea. Proc. Natl Acad. Sci. USA 105, 859-864 (2008).

[47]

Braccini, I. & Perez, S. Molecular basis of Ca(2+)-induced gelation in alginates and pectins: the egg-box model revisited. Biomacromolecules 2, 1089-1096 (2001).

[48]

Wang, N. & Qin, X. N. Effect of mineral nutrition levels on fruit splitting in Jin-Cheng orange. J. Southwest Agric. Univ. 4, 458-462 (1987).

[49]

Verslues, P. E. & Zhu, J. K. New developments in abscisic acid perception and metabolism. Curr. Opin. Plant Biol. 10, 447-452 (2007).

[50]

Saladie, M. et al. A reevaluation of the key factors that influence tomato fruit softening and integrity. Plant Physiol. 144, 1012-1028 (2007).

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