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http://dx.doi.org/10.5423/PPJ.OA.02.2018.0032

Genome-wide Identification, Classification, and Expression Analysis of the Receptor-Like Protein Family in Tomato

Kang, Won-Hee (Institute of Agriculture & Life Science, Gyeongsang National University)
Yeom, Seon-In (Institute of Agriculture & Life Science, Gyeongsang National University)

Publication Information

The Plant Pathology Journal / v.34, no.5, 2018 , pp. 435-444 More about this Journal

Abstract

Receptor-like proteins (RLPs) are involved in plant development and disease resistance. Only some of the RLPs in tomato (Solanum lycopersicum L.) have been functionally characterized though 176 genes encoding RLPs, which have been identified in the tomato genome. To further understand the role of RLPs in tomato, we performed genome-guided classification and transcriptome analysis of these genes. Phylogenic comparisons revealed that the tomato RLP members could be divided into eight subgroups and that the genes evolved independently compared to similar genes in Arabidopsis. Based on location and physical clustering analyses, we conclude that tomato RLPs likely expanded primarily through tandem duplication events. According to tissue specific RNA-seq data, 71 RLPs were expressed in at least one of the following tissues: root, leaf, bud, flower, or fruit. Several genes had expression patterns that were tissue specific. In addition, tomato RLP expression profiles after infection with different pathogens showed distinguish gene regulations according to disease induction and resistance response as well as infection by bacteria and virus. Notably, Some RLPs were highly and/or unique expressed in susceptible tomato to pathogen, suggesting that the RLP could be involved in disease response, possibly as a host-susceptibility factor. Our study could provide an important clues for further investigations into the function of tomato RLPs involved in developmental and response to pathogens.

Keywords

gene expression profiling; host-susceptibility factor; plant-microbe interaction; receptor-like protein (RLP); Solanum lycopersicum;

Citations & Related Records

Reference

1	Chen, T., Lv, Y., Zhao, T., Li, N., Yang, Y., Yu, W., He, X., Liu, T. and Zhang, B. 2013. Comparative transcriptome profiling of a resistant vs. susceptible tomato (Solanum lycopersicum) cultivar in response to infection by tomato yellow leaf curl virus. PloS one 8:e80816. DOI
2	Dixon, M. S., Jones, D. A., Keddie, J. S., Thomas, C. M., Harrison, K. and Jones, J. D. 1996. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84:451-459. DOI
3	Dixon, M. S., Hatzixanthis, K., Jones, D. A., Harrison, K. and Jones, J. D. 1998. The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 10:1915-1925. DOI
4	Dolinski, K. and Botstein, D. 2007. Orthology and functional conservation in eukaryotes. Annu. Rev. Genet. 41:465-507. DOI
5	Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. DOI
6	Finn, R. D., Clements, J. and Eddy, S. R. 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 39:W29-W37. DOI
7	Fritz-Laylin, L. K., Krishnamurthy, N., Tor, M., Sjolander, K. V. and Jones, J. D. 2005. Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis. Plant Physiol. 138:611-623. DOI
8	Hulbert, S. H., Webb, C. A., Smith, S. M. and Sun, Q. 2001. Resistance gene complexes: evolution and utilization. Annu. Rev. Phytopathol. 39:285-312. DOI
9	Jehle, A. K., Lipschis, M., Albert, M., Fallahzadeh-Mamaghani, V., Furst, U., Mueller, K. and Felix, G. 2013. The receptor-like protein ReMAX of Arabidopsis detects the microbe-associated molecular pattern eMax from Xanthomonas. Plant Cell 25:2330-2340. DOI
10	Jeong, S., Trotochaud, A. E. and Clark, S. E. 1999. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11:1925-1934. DOI
11	Jones, D. A., Thomas, C. M., Hammond-Kosack, K. E., Balint-Kurti, P. J. and Jones, J. D. 1994. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789-793. DOI
12	Jupe, F., Pritchard, L., Etherington, G. J., Mackenzie, K., Cock, P. J., Wright, F., Sharma, S. K., Bolser, D., Bryan, G. J., Jones, J. D. and Hein, I. 2012. Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genomics 13:75. DOI
13	Kang, W. H., Kim, S., Lee, H. A., Choi, D. and Yeom, S. I. 2016. Genome-wide analysis of Dof transcription factors reveals functional characteristics during development and response to biotic stresses in pepper. Sci. Rep. 6:33332. DOI
14	Kawchuk, L. M., Hachey, J., Lynch, D. R., Kulcsar, F., van Rooijen, G., Waterer, D. R., Robertson, A., Kokko, E., Byers, R., Howard, R. J., Fischer, R. and Prufer, D. 2001. Tomato Ve disease resistance genes encode cell surface-like receptors. Proc. Natl. Acad. Sci. U.S.A. 98:6511-6515. DOI
15	Kayes, J. M. and Clark, S. E. 1998. CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125:3843-3851.
16	Kim, S. B., Kang, W. H., Huy, H. N., Yeom, S. I., An, J. T., Kim, S., Kang, M. Y., Kim, H. J., Jo, Y. D., Ha, Y., Choi, D. and Kang, B. C. 2017. Divergent evolution of multiple virus-resistance genes from a progenitor in Capsicum spp. New Phytol. 213:886-899. DOI
17	Kim, Y. J., Lin, N. C. and Martin, G. B. 2002. Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589-598. DOI
18	Kruijt, M., De Kock, M. J. and de Wit, P. J. 2005. Receptor-like proteins involved in plant disease resistance. Mol. Plant Pathol. 6:85-97. DOI
19	Lee, H. A. and Yeom, S. I. 2015. Plant NB-LRR proteins: tightly regulated sensors in a complex manner. Brief. Funct. Genomics 14:233-242. DOI
20	Monaghan, J. and Zipfel, C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15:349-357. DOI
21	Nadeau, J. A. and Sack, F. D. 2002. Control of stomatal distribution on the Arabidopsis leaf surface. Science 296:1697-1700. DOI
22	Taguchi-Shiobara, F., Yuan, Z., Hake, S. and Jackson, D. 2001. The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize. Genes Dev. 15:2755-2766. DOI
23	Takken, F. L., Thomas, C. M., Joosten, M. H., Golstein, C., Westerink, N., Hille, J., Nijkamp, H. J., De Wit, P. J. and Jones, J. D. 1999. A second gene at the tomato Cf-4 locus confers resistance to cladosporium fulvum through recognition of a novel avirulence determinant. Plant J. 20:279-288. DOI
24	Thomas, C. M., Jones, D. A., Parniske, M., Harrison, K., Balint-Kurti, P. J., Hatzixanthis, K. and Jones, J. D. 1997. Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9:2209-2224. DOI
25	Tomato Genome, C. 2012. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635-641. DOI
26	Tor, M., Lotze, M. T. and Holton, N. 2009. Receptor-mediated signalling in plants: molecular patterns and programmes. J. Exp. Bot. 60:3645-3654. DOI
27	Voorrips, R. E. 2002. MapChart: software for the graphical presentation of linkage maps and QTLs. J. Hered. 93:77-78. DOI
28	Yeom, S. I., Seo, E., Oh, S. K., Kim, K. W. and Choi, D. 2012. A common plant cell-wall protein HyPRP1 has dual roles as a positive regulator of cell death and a negative regulator of basal defense against pathogens. Plant J. 69:755-768. DOI
29	Wang, G., Long, Y., Thomma, B. P. J., de Wit, P. J., Angenent, G. C. and Fiers, M. 2010. Functional analyses of the CLAVATA2-like proteins and their domains that contribute to CLAVATA2 specificity. Plant Physiol. 152:320-331. DOI
30	Wang, G., Ellendorff, U., Kemp, B., Mansfield, J. W., Forsyth, A., Mitchell, K., Bastas, K., Liu, C. M., Woods-Tor, A., Zipfel, C., de Wit, P. J., Jones, J. D., Tor, M. and Thomma, B. P. 2008. A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiol. 147:503-517. DOI
31	Yeom, S. I., Baek, H. K., Oh, S. K., Kang, W. H., Lee, S. J., Lee, J. M., Seo, E., Rose, J. K., Kim, B. D. and Choi, D. 2011. Use of a secretion trap screen in pepper following Phytophthora capsici infection reveals novel functions of secreted plant proteins in modulating cell death. Mol. Plant-Microbe Interact. 24:671-684. DOI
32	Zhang, L., Kars, I., Essenstam, B., Liebrand, T. W., Wagemakers, L., Elberse, J., Tagkalaki, P., Tjoitang, D., van den Ackerveken, G. and van Kan, J. A. 2014. Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the arabidopsis receptor-like protein Responsiveness to Botrytis Polygalacturonases 1. Plant Physiol. 164:352-364. DOI
33	Abramovitch, R. B., Kim, Y. J., Chen, S., Dickman, M. B. and Martin, G. B. 2003. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22:60-69. DOI
34	Rosli, H. G., Zheng, Y., Pombo, M. A., Zhong, S., Bombarely, A., Fei, Z., Collmer, A. and Martin, G. B. 2013. Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity. Genome Biol. 14:R139. DOI
35	Seo, E., Kim, S., Yeom, S. I. and Choi, D. 2016. Genome-Wide Comparative Analyses Reveal the Dynamic Evolution of Nucleotide-Binding Leucine-Rich Repeat Gene Family among Solanaceae Plants. Front. Plant Sci. 7:1205.
36	Shen, Y. and Diener, A. C. 2013. Arabidopsis thaliana resistance to fusarium oxysporum 2 implicates tyrosine-sulfated peptide signaling in susceptibility and resistance to root infection. PLoS Genet. 9:e1003525. DOI
37	Andolfo, G., Sanseverino, W., Rombauts, S., Van de Peer, Y., Bradeen, J. M., Carputo, D., Frusciante, L. and Ercolano, M. R. 2013. Overview of tomato (Solanum lycopersicum) candidate pathogen recognition genes reveals important Solanum R locus dynamics. New phytol. 197:223-237. DOI
38	Pan, L., Lv, S., Yang, N., Lv, Y., Liu, Z., Wu, J. and Wang, G. 2016. The Multifunction of CLAVATA2 in Plant Development and Immunity. Front. Plant Sci. 7:1573.
39	Belfanti, E., Silfverberg-Dilworth, E., Tartarini, S., Patocchi, A., Barbieri, M., Zhu, J., Vinatzer, B. A., Gianfranceschi, L., Gessler, C. and Sansavini, S. 2004. The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proc. Natl. Acad. Sci. U.S.A. 101:886-890. DOI
40	Chen, J. Y., Huang, J. Q., Li, N. Y., Ma, X. F., Wang, J. L., Liu, C., Liu, Y. F., Liang, Y., Bao, Y. M. and Dai, X. F. 2015. Genome-wide analysis of the gene families of resistance gene analogues in cotton and their response to Verticillium wilt. BMC Plant Biol. 15:148. DOI
41	Petre, B., Hacquard, S., Duplessis, S. and Rouhier, N. 2014. Genome analysis of poplar LRR-RLP gene clusters reveals RISP, a defense-related gene coding a candidate endogenous peptide elicitor. Front. Plant Sci. 5:111.
42	Ron, M. and Avni, A. 2004. The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16:1604-1615. DOI