Functional characterization of a tomato COBRA-like gene functioning in fruit development and ripening

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Cao, Ying ^a,e   Tang, Xiaofeng ^a   Giovannoni, Jim ^c   Xiao, Fangming ^d   Liu, Yongsheng ^a,b  

^a SICHUAN UNIVERSITY   (China)

^b HEFEI UNIVERSITY OF TECHNOLOGY   (China)

^c Boyce Thompson Institute for Plant Research   (United States)

^d UNIVERSITY OF IDAHO   (United States)

^e SOUTHWEST UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; LYCOPERSICON ESCULENTUM;

VEGETABLE PROTEIN;

ARTICLE; CELL WALL; CYTOLOGY; FRUIT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; INFRARED SPECTROSCOPY; MACROMOLECULE; METABOLISM; MULTIGENE FAMILY; PHENOTYPE; PHYLOGENY; PLANT EPIDERMIS; PLANT GENE; SIGNAL TRANSDUCTION; TOMATO; TRANSGENIC PLANT; UPREGULATION;

CELL WALL; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; LYCOPERSICON ESCULENTUM; MACROMOLECULAR SUBSTANCES; MULTIGENE FAMILY; PHENOTYPE; PHYLOGENY; PLANT EPIDERMIS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; UP-REGULATION;

MLCS; MLOWN;

EID: 84868535320     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-211     Document Type: Article

References (58)

1. Giovannoni JJ. Genetic regulation of fruit development and ripening. Plant Cell 2004, 16:S170-S180. 10.1105/tpc.019158, 2643394, 15010516.
2. Meli VS, Ghosh S, Prabha TN, Chakraborty N, Chakraborty S, Datta A. Enhancement of fruit shelf life by N-glycan processing enzymes. Proc Natl Acad Sci USA 2010, 6:2413-2418.
3. Brummell DA, Harpster MH. Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 2001, 347:311-340.
4. Toivonen PMA, Brummell DA. Biochemical bases of appearance and texture changes in fresh-cut fruit and vegetables. Postharvest Biol Technol 2008, 48:1-14.
5. Sheehy RE, Kramer M, Hiatt WR. Reduction of polygalacturonase activity in tomato fruit by antisense RNA. Proc Natl Acad Sci USA 1988, 85:8805-8809. 10.1073/pnas.85.23.8805, 282595, 16593997.
6. Giovannoni JJ, DellaPenna D, Bennett A, Fischer R. Expression of a chimeric polygalacturonase gene in transgenic rin (ripening inhibitor) tomato fruit results in polyuronide degradation but not fruit softening. Plant Cell 1989, 1:53-63. 159736, 2535467.
7. Tieman DM, Harriman RW, Ramamohan G, Handa AK. An antisense pectin methylesterase gene alters pectin chemistry and soluble solids in tomato fruit. Plant Cell 1992, 4:667-679. 160163, 12297658.
8. Smith DL, Gross KC. A family of at least seven β-galactosidase genes is expressed during tomato fruit development. Plant Physiol 2000, 123:1173-1183. 10.1104/pp.123.3.1173, 59080, 10889266.
9. Rose JKC, Lee HH, Bennett AB. Expression of a divergent expansin gene is fruit-specific and ripening-regulated. Proc Natl Acad Sci USA 1997, 94:5955-5960. 10.1073/pnas.94.11.5955, 20888, 9159182.
10. Brummell DA, Harpster MH, Civello PM, Palys JM, Bennett AB, Dunsmuir P. Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell 1999, 11:2203-2216. 144123, 10559444.
11. Smith DL, Starrett DA, Gross KC. A gene coding for tomato fruit β-galactosidase II is expressed during fruit ripening. Plant Physiol 1998, 117:417-423. 10.1104/pp.117.2.417, 34961, 9625694.
12. Tieman DM, Handa AK. Reduction in pectin methylesterase activity modifies tissue integrity and cation levels in ripening tomato (Lycopersicon esculentum Mill.) fruits. Plant Physiol 1994, 106:429-436. 159547, 12232340.
13. Suvarnalatha G, Prabha TN. α-d-Mannosidase from Lycopersicon esculentum Mill. Phytochemistry 1999, 7:1111-1115.
14. Cosgrove DJ. Loosening of plant cell walls by expansins. Nature 2000, 407:321-326. 10.1038/35030000, 11014181.
15. Cho HT, Cosgrove DJ. Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 2000, 97:9783-9788. 10.1073/pnas.160276997, 16942, 10931949.
16. Brummell DA, Howie WJ, Ma C, Dunsmuir P. Postharvest fruit quality of transgenic tomatoes suppressed in expression of a ripening-related expansin. Postharvest Biology and Technolog 2002, 25:209-220.
17. Schindelman G, Morikami A, Jung J, Baskin TI, Carpita NC, Derbyshire P, McCann MC, Benfey1 PN. COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev 2001, 15:1115-1127. 10.1101/gad.879101, 312689, 11331607.
18. Li Y, Qian Q, Zhou Y, Yan M, Sun L, Zhang M, Fu Z, Wang Y, Han B, Pang X, Chen M, Li J. BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell 2003, 15:2020-2031. 10.1105/tpc.011775, 181328, 12953108.
19. Brown DM, Zeef LAH, Ellis J, Goodacre R, Turner SR. Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 2005, 17:2281-2295. 10.1105/tpc.105.031542, 1182489, 15980264.
20. Ching A, Dhugga KS, Appenzeller L, Meeley B, Bourret TM, Howard RJ, Rafalski A. Brittle stalk 2 encodes a putative glycosylphosphatidylinositol-anchored protein that affects mechanical strength of maize tissues by altering the composition and structure of secondary cell. Planta 2006, 224:1174-1184. 10.1007/s00425-006-0299-8, 16752131.
21. Roudier F, Schindelman G, DeSalle R, Benfey PN. The COBRA family of putative GPI-anchored proteins in Arabidopsis: a new fellowship in expansion. Plant Physiol 2002, 130:538-548. 10.1104/pp.007468, 166585, 12376623.
22. Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GH, Schindelman G, Song S, Baskin TI, Dupree P, Wasteneys GO, Benfey PN. COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 2005, 17:1749-1763. 10.1105/tpc.105.031732, 1143074, 15849274.
23. Hauser MT, Morikami A, Benfey PN. Conditional root expansion mutants of Arabidopsis. Development 1995, 121:237-1252.
24. Sindhu A, Langewisch T, Olek A, Multani DS, McCann MC, Vermerris W, Carpita NC, Johal G. Maize brittle stalk2 encodes a COBRA-Like protein expressed in early organ development but required for tissue flexibility at maturity. Plant Physiol 2007, 145:1444-1459. 10.1104/pp.107.102582, 2151699, 17932309.
25. Santino CG, Stanford GL, Conner TW. Developmental and transgenic analysis of two tomato fruit enhanced genes. Plant Mol Biol 1997, 3:405-416.
26. 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 Experimental Botany 2005, 413:1049-1060.
27. Tsuboi M. Infrared spectrum and crystal structure of cellulose. J Polym Sci 1957, 25:159-171.
28. O'Connor RT, DuPre EF, Mitcham D. Applications of infrared absorption spectroscopy to investigations of cotton and modified cottons. Part I: Physical and crystalline modifications and oxidation. Textile Res J 1958, 28:382-392.
29. Kemsley EK. Chemometric methods for classification problems. In discriminant analysis and modelling of spectroscopic data 1998, 1-47. Chichester, UK: John Wiley.
30. Updegraff DM. Semimicro determination of cellulose in biological materials. Anal Biochem 1969, 32:420-424. 10.1016/S0003-2697(69)80009-6, 5361396.
31. Rose JKC, Hadfield KA, Labavitch JM, Bennett AB. Temporal sequence of cell wall disassembly in rapidly ripening melon fruit. Plant Physiol 1998, 117:345-361. 10.1104/pp.117.2.345, 34955, 9625688.
32. Blakeney AB, Harris PJ, Henry RJ, Stone BA. A simple and rapid preparation of alditol acetates for monosaccharide analysis. Carbohydr Res 1983, 113:291-299.
33. Brady SM, Song S, Dhugga KS, Rafalski JA, Benfey PN. Combining expression and comparative evolutionary analysis: the COBRA gene family. Plant Physiol 2007, 143:172-187. 1761980, 17098858.
34. Parker JS, Cavell AC, Dolan L, Roberts K, Grierson CS. Genetic interactions during root hair morphogenesis in Arabidopsis. Plant Cell 2000, 12:1961-1974. 149133, 11041890.
35. Jones MA, Raymond MJ, Smirnoff N. Analysis of the root hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis. Plant J 2006, 45:83-100. 10.1111/j.1365-313X.2005.02609.x, 16367956.
36. Hochholdinger F, Wen TJ, Zimmermann R, Chimot-Marolle P, ESilva O, Bruce W, Lamkey KR, Wienand U, Schnable PS. he maize (Zea mays L.) roothairless 3 gene encodes a putative GPI-anchored, monocot-specific, COBRA-like protein that significantly affects grain yield. Plant J 2008, 54:888-898. 10.1111/j.1365-313X.2008.03459.x, 2440564, 18298667.
37. Dai X, You C, Wang L, Chen G, Zhang Q, Wu C. Molecular characterization, expression pattern, and function analysis of the OsBC1L family in rice. Plant Mol Biol 2009, 71:469-481. 10.1007/s11103-009-9537-3, 19688299.
38. Bosca S, Barton CJ, Taylor NG, Ryden P, Neumetzler L, Pauly M, Roberts K, Seifert GJ. Interactions between MUR10/CesA7-dependent secondary cellulose biosynthesis and primary cell wall structure. Plant Physiol 2006, 142:1353-1363. 10.1104/pp.106.087700, 1676063, 17041031.
39. Della Penna D, Kates DS, Bennett AB. Polygalacturonase gene expression in Rutgers, rin, nor, and Nr tomato fruits. Plant Physiol 1987, 85:502-507. 10.1104/pp.85.2.502, 1054285, 16665727.
40. Harriman RW, Tieman DM, Handa AK. Molecular cloning of tomato pectin methylesterase gene and its expression in Rutgers, ripening inhibitor, nonripening, and Never Ripe tomato fruits. Plant Physiol 1991, 97:80-87. 10.1104/pp.97.1.80, 1080966, 16668419.
41. Ray J, Knapp J, Grierson D, Bird C, Schuch W. Identification and sequence determination of a cDNA clone for tomato pectinesterase. Eur J Biochem 1988, 174:119-124. 10.1111/j.1432-1033.1988.tb14070.x, 3371355.
42. Ringli C. Monitoring the outside: cell wall-sensing mechanisms. Plant Physiol 2010, 153:1445-1452. 10.1104/pp.110.154518, 2923904, 20508141.
43. Seifert GJ, Blaukopf C. Irritable walls: the plant extracellular matrix and signaling. Plant Physiol 2010, 153:467-478. 10.1104/pp.110.153940, 2879813, 20154095.
44. Showalter AM. Arabinogalactan-proteins: structure, expression and function. Cell Mol Life Sci 2001, 58:1399-1417. 10.1007/PL00000784, 11693522.
45. Yang J, Sardar HS, McGovern KR, Zhang YZ, Showalter AM. Alysine-rich arabinogalactan protein in Arabidopsis is essential for plant growth and development, including cell division and expansion. Plant J 2007, 49:629-640. 10.1111/j.1365-313X.2006.02985.x, 17217456.
46. Driouich A, Baskin TI. Intercourse between cell wall and cytoplasm exemplified by arabinogalactan proteins and cortical microtubules. Am J Bot 2008, 95:1491-1497. 10.3732/ajb.0800277, 21628156.
47. Carpita N, Tierney M, Campbell M. Molecular biology of the plant cell wall: Searching for the genes that define structure, architecture and dynamics. Plant Mol Biol 2001, 47:1-5. 10.1023/A:1010603527077, 11554466.
48. Guillon F, Philippe S, Bouchet B, Devaux M, Frasse P, Jones B, Bouzayen M, Lahaye M. Down-regulation of an auxin response factor in the tomato induces modification of fine pectin structure and tissue architecture. J Experimental Botany 2008, 59:273-288.
49. Bendtsen JD, Nielsen H, Heijne G, Brunak S. Improved prediction of signal peptides: Signal P 3.0. J Mol Biol 2004, 340:783-795. 10.1016/j.jmb.2004.05.028, 15223320.
50. Eisenhaber B, Bork P, Eisenhaber F. Sequence properties of GPI-anchored proteins near the omega-site: constraints for the polypeptide binding site of the putative transamidase. Protein Eng 1998, 11:1155-1161. 10.1093/protein/11.12.1155, 9930665.
51. Gough J, Karplus K, Hughey R, Chothia C. Assignment of homology to genome sequences using a library of Hidden Markov Models that represent all proteins of known structure. J Mol Biol 2001, 313:903-919. 10.1006/jmbi.2001.5080, 11697912.
52. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25:4876-4882. 10.1093/nar/25.24.4876, 147148, 9396791.
53. Kumar S, Tamura K, Jakobsen IB, Nei M. MEGA2: Molecular evolutionary genetics analysis software. Bioinformatics 2001, 17:1244-1245. 10.1093/bioinformatics/17.12.1244, 11751241.
54. Fillatti JJ, Kiser J, Rose R, Comai L. Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Bio Technology 1987, 5:726-730.
55. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (RESTa) for group-wise comparison and statistical analysis if relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:36.
56. Blumenkrantz N, Asboe-Hansen G. New method for quantitative determination of uronic acids. Anal Biochem 1973, 54:484-489. 10.1016/0003-2697(73)90377-1, 4269305.
57. McCann M, Chen L, Roberts K, Kemsley EK, Séné C, Carpita NC, Stacey NJ, Wilson RH. Infrared microspectroscopy: Sampling heterogeneity in plant cell wall composition and architecture. Physiol Plant 1997, 100:729-738.
58. Liang CY, Marchessault RH. Infrared spectra of crystalline polysaccharides. II. Native celluloses in the region from 640 to 1700 cm-1. J Polym Sci 1959, 39:269-278.