In Silico Prediction of Cell Wall Remodeling Genes in Tomato, Banana, Melon and Grape

Abstract

Ripening is a complex developmental process and involves many events such as textural and constitutional changes. The texture of fleshy fruits is one of the major criteria for consumer choice. However, the molecular determinants of ripening- associated changes in texture or “softening” are relatively poorly understood and seem to involve a large number of cell wall remodelling factors. The recent completion of the tomato genome sequence has revealed more than 50 cell wall structure-related genes that are expressed during fruit development and ripening and may impact texture changes in this fruit. The aim of the project is to compare, on a genome-wide scale, ripening-related gene expression in a range of fleshy fruits and especially those linked with cell wall remodelling. Then by identifying orthologous genes in different fruit species to make predictions about those genes likely to important for the softening process in all fleshy fruits. Comparative genomics analysis of tomato (Solanum lycopersicum), banana (Musa acuminate), melon (Cucumis melo) and grape (Vitis vinifera), has been undertaken using Inparanoid, Multiparanoid and BLAST2GO software. This analysis showed that a total of 8,982 (25.86%) gene models could be identified in common between all four genomes based on comparison of amino acid sequences. Of these genes, 262 in tomato, 252 in grape, 261 in melon, and 198 in banana were identified as encoding cell wall structure-related proteins. However, comparison of the expression patterns of these genes revealed that most were expressed in tissues other than ripening fruits, and of the fruit expressed genes only a small number were common between different fruit species. This in silico analysis should provide additional clues as a target for manipulation of fruit softening in a range of fleshy fruit species. These also provide new opportunities to develop varieties of tomatoes that can survive the trip from the farm to the grocery store whilst maintaining excellent flavour and shelf-life.

Keywords

• comparative genomics
• inparanoid
• cell wall

Supporting Institution

International Islamic University Malaysia (IIUM)

Project Number

RIGS17-022-0597

Thanks

I wish to thank International Islamic University Malaysia (IIUM) Research Initiative Grant Scheme (RIGS17-022-0597) for sponsored this work and The University of Nottingham UK for providing the facilities and technical assistant.

References

1. Altschul, S., W. Gish, W. Miller, E. Myers, and D. Lipman. "Basic local alignment search tool Journal of Molecular Biology 215 (3), 403–410.
2. Ashburner, Michael, Catherine A. Ball, Judith A. Blake, David Botstein, Heather Butler, J. Michael Cherry, Allan P. Davis et al. "Gene ontology: tool for the unification of biology." Nature genetics 25, no. 1 (2000): 25.
3. Atkinson, Ross G., Paul W. Sutherland, Sarah L. Johnston, Kularajathevan Gunaseelan, Ian C. Hallett, Deepali Mitra, David A. Brummell, Roswitha Schröder, Jason W. Johnston, and Robert J. Schaffer. "Down-regulation of POLYGALACTURONASE1 alters firmness, tensile strength and water loss in apple (Malus x domestica) fruit." BMC plant biology 12, no. 1 (2012): 129.
4. Chothia, Cyrus, and Arthur M. Lesk. "The relation between the divergence of sequence and structure in proteins." The EMBO journal 5, no. 4 (1986): 823-826.
5. Conesa, Ana, Stefan Götz, Juan Miguel García-Gómez, Javier Terol, Manuel Talón, and Montserrat Robles. "Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research." Bioinformatics 21, no. 18 (2005): 3674-3676.
6. Delmer, Deborah P., and Candace H. Haigler. "The regulation of metabolic flux to cellulose, a major sink for carbon in plants." Metabolic engineering 4, no. 1 (2002): 22-28
7. D’hont, Angélique, France Denoeud, Jean-Marc Aury, Franc-Christophe Baurens, Françoise Carreel, Olivier Garsmeur, Benjamin Noel et al. "The banana (Musa acuminata) genome and the evolution of monocotyledonous plants." Nature 488, no. 7410 (2012): 213.
8. Doolittle, Russell F. "Similar amino acid sequences: chance or common ancestry?." Science 214, no. 4517 (1981): 149-159.

9. García, Juan M., Sara Posé, Juan Muñoz-Blanco, Miguel A. Quesada, and José A. Mercado. "The polygalacturonase FaPG1 gene plays a key role in strawberry fruit softening." Plant signaling & behavior 4, no. 8 (2009): 766-768.
10. Garcia-Mas, Jordi, Andrej Benjak, Walter Sanseverino, Michael Bourgeois, Gisela Mir, Víctor M. González, Elizabeth Hénaff et al. "The genome of melon (Cucumis melo L.)." Proceedings of the National Academy of Sciences 109, no. 29 (2012): 11872-11877.
11. Goulao, Luis F., and Cristina M. Oliveira. "Cell wall modifications during fruit ripening: when a fruit is not the fruit." Trends in Food Science & Technology 19, no. 1 (2008): 4-25.
12. Jaillon, Olivier, Jean-Marc Aury, Benjamin Noel, Alberto Policriti, Christian Clepet, Alberto Casagrande, Nathalie Choisne et al. "The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla." nature 449, no. 7161 (2007): 463.
13. Jiménez-Bermudez, Silvia, José Redondo-Nevado, Juan Munoz-Blanco, José L. Caballero, José M. López-Aranda, Victoriano Valpuesta, Fernando Pliego-Alfaro, Miguel A. Quesada, and José A. Mercado. "Manipulation of strawberry fruit softening by antisense expression of a pectate lyase gene." Plant physiology 128, no. 2 (2002): 751-759.
14. Marín‐Rodríguez, M. Celia, John Orchard, and Graham B. Seymour. "Pectate lyases, cell wall degradation and fruit softening." Journal of experimental botany 53, no. 377 (2002): 2115-2119.
15. Mbéguié-A-Mbéguié, D., O. Hubert, F. C. Baurens, T. Matsumoto, M. Chillet, B. Fils-Lycaon, and S. Sidibé-Bocs. "Expression patterns of cell wall-modifying genes from banana during fruit ripening and in relationship with finger drop." Journal of Experimental Botany 60, no. 7 (2009): 2021-2034.
16. Nei, Masatoshi, and Arun K. Roychoudhury. "Probability of fixation of nonfunctional genes at duplicate loci." The American Naturalist 107, no. 955 (1973): 362-372.
17. Campos-Vargas, Reinaldo, and Ariel Orellana. "Assessment of Prunus persica fruit softening using a proteomics approach." Journal of proteomics 75, no. 5 (2012): 1618-1638.
18. Ohno, Susumu. Evolution by gene duplication. Springer Science & Business Media, 2013.
19. O'brien, Kevin P., Maido Remm, and Erik LL Sonnhammer. "Inparanoid: a comprehensive database of eukaryotic orthologs." Nucleic acids research 33, no. suppl_1 (2005): D476-D480.
20. Petrov, D. A., and D. L. Hartl. "Pseudogene evolution and natural selection for a compact genome." Journal of Heredity 91, no. 3 (2000): 221-227.
21. Remm, Maido, Christian EV Storm, and Erik LL Sonnhammer. "Automatic clustering of orthologs and in-paralogs from pairwise species comparisons." Journal of molecular biology 314, no. 5 (2001): 1041-1052.
22. Shulaev, Vladimir, Daniel J. Sargent, Ross N. Crowhurst, Todd C. Mockler, Otto Folkerts, Arthur L. Delcher, Pankaj Jaiswal et al. "The genome of woodland strawberry (Fragaria vesca)." Nature genetics 43, no. 2 (2011): 109.
23. Stein, Lincoln. "Genome annotation: from sequence to biology." Nature reviews genetics 2, no. 7 (2001): 493.
24. Seymour, Graham B., Lars Østergaard, Natalie H. Chapman, Sandra Knapp, and Cathie Martin. "Fruit development and ripening." Annual review of plant biology 64 (2013): 219-241.
25. Tomato Genome Consortium. "The tomato genome sequence provides insights into fleshy fruit evolution." Nature 485, no. 7400 (2012): 635.
26. Uluisik, Selman, Natalie H. Chapman, Rebecca Smith, Mervin Poole, Gary Adams, Richard B. Gillis, Tabot MD Besong et al. "Genetic improvement of tomato by targeted control of fruit softening." Nature biotechnology 34, no. 9 (2016): 950.
27. Velasco, Riccardo, Andrey Zharkikh, Jason Affourtit, Amit Dhingra, Alessandro Cestaro, Ananth Kalyanaraman, Paolo Fontana et al. "The genome of the domesticated apple (Malus× domestica Borkh.)." Nature genetics 42, no. 10 (2010): 833.