Abstract
cDNA clones encoding homologues of expansins, a class of cell wall proteins involved in cell wall modification, were isolated from various stages of growing and ripening fruit of tomato (Lycopersicon esculentum). cDNAs derived from five unique expansin genes were obtained, termed tomato Exp3 to Exp7, in addition to the previously described ripening-specific tomato Exp1 (Rose et al. (1997) Proc Natl Acad Sci USA 94: 5955–5960). Deduced amino acid sequences of tomato Exp1, Exp4 and Exp6 were highly related, whereas Exp3, Exp5 and Exp7 were more divergent. Each of the five expansin genes showed a different and characteristic pattern of mRNA expression. mRNA of Exp3 was present throughout fruit growth and ripening, with highest accumulation in green expanding and maturing fruit, and lower, declining levels during ripening. Exp4 mRNA was present only in green expanding fruit, whereas Exp5 mRNA was present in expanding fruit but had highest levels in full-size maturing green fruit and declined during the early stages of ripening. mRNAs from each of these genes were also detected in leaves, stems and flowers but not in roots. Exp6 and Exp7 mRNAs were present at much lower levels than mRNAs of the other expansin genes, and were detected only in expanding or mature green fruit. The results indicate the presence of a large and complex expansin gene family in tomato, and suggest that while the expression of several expansin genes may contribute to green fruit development, only Exp1 mRNA is present at high levels during fruit ripening.
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References
Arrowsmith DA, de Silva J: Characterisation of two tomato fruit-expressed cDNAs encoding xyloglucan endotransglycosylase. Plant Mol Biol 28: 391–403 (1995).
Brummell DA, Labavitch JM: Effect of antisense suppression of endopolygalacturonase activity on polyuronide molecular weight in ripening tomato fruit and in fruit homogenates. Plant Physiol 115: 717–725 (1997).
Carpita NC, Gibeaut DM: Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3: 1–30 (1993).
Cho H-T, Kende H: Expansins in deepwater rice internodes. Plant Physiol 113: 1137–1143 (1997).
Cho H-T, Kende H: Expansins and internodal growth of deepwater rice. Plant Physiol 113: 1145–1151 (1997).
Cho H-T, Kende H: Expression of expansin genes is correlated with growth in deepwater rice. Plant Cell 9: 1661–1671 (1997).
Cosgrove DJ: Wall extensibility: its nature, measurement and relationship to plant cell growth. New Phytol 124: 1–23 (1993).
Cosgrove DJ: Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol 13: 171–201 (1997).
Cosgrove DJ, Bedinger P, Durachko DM: Group I allergens of grass pollen as cell wall-loosening agents. Proc Natl Acad Sci USA 94: 6559–6564 (1997).
Dunsmuir P, Bond D, Lee K, Godoni D, Townsend J: The expression of introduced genes in regenerated plants. In: Gelvin SB, Schilperoort RA (eds) Plant Molecular Biology Manual, pp. 45–59. Kluwer Academic Publishers, Dordrecht, Netherlands (1987).
Fleming AJ, McQueen-Mason S, Mandel T, Kuhlemeier C: Induction of leaf primordia by the cell wall protein expansin. Science 276: 1415–1418 (1997).
Fry SC, Smith RC, Renwick KF, Martin DJ, Hodge SK, Matthews KJ: Xyloglucan endotransglycosylase, a new wallloosening enzyme activity from plants. Biochem J 282: 821–828 (1992).
Gillaspy G, Ben-David H, GruissemW: Fruits: a developmental perspective. Plant Cell 5: 1439–1451 (1993).
Giovannoni JJ, DellaPenna D, Bennett AB, Fischer RL: Expression of a chimeric polygalacturonase gene in transgenic rin (ripening inhibitor) tomato fruit results in polyuronide degradation but not fruit softening. Plant Cell 1: 53–63 (1989).
Gonzalez-Bosch C, Brummell DA, Bennett AB: Differential expression of two endo-1,4-β-glucanase genes in pericarp and locules of wild-type and mutant tomato fruit. Plant Physiol 111: 1313–1319 (1996).
Greene B, Walko R, Hake S: Mutator insertions in an intron of the maize knotted1 gene result in dominant suppressible mutations. Genetics 138: 1275–1285 (1994).
Hayashi T, Wong Y-S, Maclachlan G: Pea xyloglucan and cellulose. II. Hydrolysis by pea endo-1,4-β-glucanase. Plant Physiol 75: 605–610 (1984).
Higgins DG, Bleasby AJ, Fuchs R: CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci 8: 189–191 (1992).
Hobson GE: Cellulase activity during the maturation and ripening of tomato fruit. J Food Sci 33: 588–592 (1968).
Hobson GE, Grierson D: Tomato. In: Seymour GB, Taylor JE, Tucker GA (eds) Biochemistry of Fruit Ripening, pp. 405–442. Chapman and Hall, London (1993).
Huber DJ, O'Donoghue EM: Polyuronides in avocado (Persea americana) and tomato (Lycopersicon esculentum) fruits exhibit markedly different patterns of molecular weight downshifts during ripening. Plant Physiol 102: 473–480 (1993).
Keller E, Cosgrove DJ: Expansins in growing tomato leaves. Plant J 8: 795–802 (1995).
Kramer M, Sanders R, Bolkan H, Waters C, Sheehy RE, Hiatt WR: Postharvest evaluation of transgenic tomatoes with reduced levels of polygalacturonase: processing, firmness and disease resistance. Postharvest Biol Technol 1: 241–255 (1992).
Langley KR, Martin A, Stenning R, Murray AJ, Hobson GE, Schuch WW, Bird CR: Mechanical and optical assessment of the ripening of tomato fruit with reduced polygalacturonase activity. J Sci Food Agric 66: 547–554 (1994).
Li Z-C, Durachko DM, Cosgrove DJ: An oat coleoptile wall protein that induces wall extension in vitro and that is antigeni169 cally related to a similar protein from cucumber hypocotyls. Planta 191: 349–356 (1993).
Maclachlan G, Brady C: Endo-1,4-β-glucanase, xyloglucanase and xyloglucan endo-transglycosylase activities versus potential substrates in ripening tomatoes. Plant Physiol 105: 965–974 (1994).
McQueen-Mason SJ, Cosgrove DJ: Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci USA 91: 6574–6578 (1994).
McQueen-Mason SJ, Cosgrove DJ: Expansin mode of action on cell walls. Analysis of wall hydrolysis, stress relaxation, and binding. Plant Physiol 107: 87–100 (1995).
McQueen-Mason S, Durachko DM, Cosgrove DJ: Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4: 1425–1433 (1992).
McQueen-Mason SJ, Fry SC, Durachko DM, Cosgrove DJ: The relationship between xyloglucan endotransglycosylase and in vitro cell wall extension in cucumber hypocotyls. Planta 190: 327–331 (1993).
Michael AJ: A cDNA from pea petals with sequence similarity to pollen allergen, cytokinin-induced and genetic tumourspecific genes: identification of a new family of related sequences. Plant Mol Biol 30: 219–224 (1996).
Rose JKC, Lee HH, Bennett AB: Expression of a divergent expansin gene is fruit-specific and ripening-regulated. Proc Natl Acad Sci USA 94: 5955–5960 (1997).
Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).
Shcherban TY, Shi J, Durachko DM, Guiltinan MJ, McQueen-Mason SJ, Shieh M, Cosgrove DJ: multigene family of proteins that mediate cell wall extension in plants. Proc Natl Acad Sci USA 92: 9245–9249 (1995).
Smith CJS, Watson CF, Ray J, Bird CR, Morris PC, Schuch W, Grierson D: Antisense RNA inhibition of polygalacturonase gene expression in transgenic tomatoes. Nature 334: 724–726 (1988).
Swofford DL: PAUP: Phylogenetic Analysis Using Parsimony, vers. 3.1.1. Illinois Natural History Survey, Champaign, IL (1993).
Tong CBS, Gross KC: Glycosyl-linkage composition of tomato fruit cell wall hemicellulosic fractions during ripening. Physiol Plant 74: 365–370 (1988).
von Heijne G: A new method for predicting signal sequence cleavage sites. Nucl Acids Res 14: 4683–4690 (1986).
Wu Y, Sharp RE, Durachko DM, Cosgrove DJ: Growth maintenance of the maize primary root at low water potentials involves increases in cell-wall extension properties, expansin activity, and wall susceptibility to expansins. Plant Physiol 111: 765–772 (1996).
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Brummell, D.A., Harpster, M.H. & Dunsmuir, P. Differential expression of expansin gene family members during growth and ripening of tomato fruit. Plant Mol Biol 39, 161–169 (1999). https://doi.org/10.1023/A:1006130018931
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DOI: https://doi.org/10.1023/A:1006130018931