MD. ZAHERUL ISLAM, SOON YOUNG AHN, HAE KEUN YUN

Analysis of structure and differential expression of Pseudomonas syringae 5-like(RPS5-like) genes in pathogen-infected Vitis flexuosa

Abstract: Nucleotide binding site-leucine-rich repeat (NBS-LRR) genes are the largest gene resistance family in plants. Resistance to Pseudomonas syringae 5 (RPS5) is a member of the NBS-LRR family. RPS5 and its homologs are important disease resistance genes in plants including Arabidopsis. This study identified nine loci of RPS5-like genes in Vitis flexuosa that showed differential expression from transcriptome analysis by next generation sequencing (NGS) of V. flexuosa infected with Elsinoe ampelina based on structural analyses: VfRPS5-like1059 (Vitis flexuosa resistance to Pseudomonas syringae 5-like 1059), VfRPS5-like1833, VfRPS5-like4135, VfRPS5-like4833, VfRPS5-like6172, VfRPS5-like13564, VfRPS5-like20585, VfRPS5-like55532, and VfRPS5-like62178. These genes, 2236-4762 bp in length, exhibited the structure of a coiled coil-nucleotide binding site-leucine-rich repeat (CC-NBS-LRR) resistance gene. The predicted amino acid sequences of all nine genes contained typical NBS domains. Chromosomal localization revealed that the nine genes were located in six chromosomes of the V. flexuosa pseudo-genome. Of the nine loci, only VfRPS5-like55532 showed upregulated expression against all tested pathogens at all tested time points, except 24 h postinoculation (hpi) for E. ampelina. All tested genes also showed differential expression against major grapevine fungal and bacterial pathogens. The results presented herein will also serve as a useful reference dataset for functional analysis and utilization in molecular breeding of resistant grapevines.

Anahtar Kelimeler:

R-gene, Vitis, resistance to Pseudomonas syringae 5, Elsinoe ampelina, Rhizobium vitis, Botrytis cinerea, Colletotrichum gloesporioides, Colletotrichum acutatum, CC-NBS-LRR

Analysis of structure and differential expression of Pseudomonas syringae 5-like(RPS5-like) genes in pathogen-infected Vitis flexuosa

Keywords:

R-gene, Vitis, resistance to Pseudomonas syringae 5, Elsinoe ampelina, Rhizobium vitis, Botrytis cinerea, Colletotrichum gloesporioides, Colletotrichum acutatum, CC-NBS-LRR,

PDF

___

Ade J, DeYoung BJ, Golstein C, Innes RW (2007). Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. P Natl Acad Sci USA 104: 2531–2536.
Ahn SY, Kim SA, Jo SH, Yun HK (2014). De novo transcriptome analysis of Vitis flexuosa grapevine inoculated with Elsinoe ampelina. Plant Genet Resour-C 12: S130–S133.
Arya P, Kumar G, Acharya V, Singh AK (2014). Genome-wide identification and expression analysis of NBS-encoding genes in Malus × domestica and expansion of NBS genes family in Rosaceae. PLoS ONE 9: e107987.
Bai J, Penill LA, Ning J, Lee SW, Ramalingum J, Tian D (2002). Diversity of nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12: 1871–1884.
Baker B, Zambriski P, Dinesh-Kumar SP (1997). Signaling in plantmicrobe interactions. Science 276: 726–733.
Barka EA, Belarbi A, Hachet C, Nowak J, Audran J (2000). Enhancement of in vitro growth and resistance to gray mould of Vitis vinifera co-cultured with plant growth-promoting rhizobacteria. FEMS Microbiol Lett 186: 91–95.
Bella J, Hindle KL, McEwan PA, Lovell SC (2008). The leucine-rich repeat structure. Cell Mol Life Sci 65: 2307–2333.
Burkhard P, Stetefeld J, Strelkov SV (2001). Coiled-coils: a highly versatile protein folding motif. Trends Cell Biol 11: 81–82.
Chang S, Puryear J, Cairney J (1993). A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol 11: 113–116.
De Waard MA, Georgopoulos SG, Hollomon DW, Ishii H, Leroux P, Ragsdale NN, Schwinn FJ (1993). Chemical control of plant diseases: problems and prospects. Annu Rev Phytopathol 31: 403–421.
Dong X (2001). Genetic dissection of systemic acquired resistance. Curr Opin Plant Biol 4: 309–314.
Eastwell KC, Sholberg PL, Sayler RJ (2006). Characterizing potential bacterial biocontrol agents for suppression of Rhizobium vitis, causal agent of crown gall disease in grapevines. Crop Prot 25: 1191–1200.
Eibach R, Diehl H, Alleweldt G (1989). Untersuchungen zur vererbung von resistenzeigenschaften bei reben gegen Oidium tuckeri, Plasmopara viticola and Botrytis cinerea. Vitis 28: 209– 228.
Felsenstein J (1985). Confidence limits on phylogenesis: an approach using the bootstrap. Evolution 39: 783–791.
Gong C, Cao S, Fan R, Wei B, Chen G, Wang X, Li Y, Zhang X (2013). Identification and phylogenetic analysis of a CC-NBS-LRR encoding gene assigned on chromosome 7B of wheat. Int J Mol Sci 14: 15330–15347.
Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW, Dangl JL (1995). Structure of the Arabidopsis RPM1 gene enabling duel specificity disease resistance. Science 269: 843–846.
Gullino M (1992). Chemical control of Botrytis spp. In: Verhoeff K, Malathrakis NE, Williamson B, editors. Recent Advances in Botrytis Research. Wageningen, the Netherlands: Pudoc Scientific Publishers, pp. 217–222.
Guruprasad K, Reddy BV, Pandit MW (1990). Correlation between stability of a protein and its dipeptide composition: a novel approach for predicting in vivo stability of a protein from its primary sequence. Protein Eng 4: 155–161.
Gururani MA, Venkatesh J, Upadhyaya CP, Nookaraju A, Pandey SK, Park SW (2012). Plant disease resistance genes: current status and future directions. Physiol Mol Plant Pathol 78: 51–65.
Halterman DA, Wei F, Wise RP (2003). Powdery mildew-induced Mla mRNAs are alternatively spliced and contain multiple upstream open reading frames. Plant Physiol 131: 558–567.
Hammond-Kosack KE, Jones JD (1996). Resistance gene-dependent plant defense responses. Plant Cell 8: 1773–1791.
Hammond-Kosack KE, Jones JD (2000). Response to plant pathogen. In: Buchanan BB, Gruissem W, Jones RL, editors. Biochemistry and Molecular Biology of Plants. Rockville, MD, USA: American Society of Plant Physiologists, pp. 1102–1156.
Hammond-Kosack KE, Jones JDG (1997). Plant disease resistance genes. Annu Rev Plant Physiol 48: 573–605.
He B, Huang X, Li D, Jiang C, Yu T, Yin F, Li W, Cheng Z (2013). The cDNA cloning of a novel bacterial blight-resistance gene ME137. Acta Bioch Bioph Sin 45: 422–424.
Hong SK, Kim WG, Yun HK, Choi KJ (2008). Morphological variations, genetic diversity and pathogenicity of Colletotrichum species causing grape ripe rot in Korea. Plant Pathology J 24: 269–278.
Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C et al. (2007). The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463–467.
Joshi RK, Nayak S (2011). Functional characterization and signal transduction ability of nucleotide-binding site-leucine-rich repeat resistance genes in plants. Genet Mol Res 10: 2637–2652.
Kar B, Nanda S, Nayak PK, Nayak S, Joshi RK (2013). Molecular characterization and functional analysis of CzR1, a coiledcoil-nucleotide-binding-site-leucine-rich repeat R-gene from Curcuma zedoaria Loeb. that confers resistance to Pythium aphanidermatum. Physiol Mol Plant Pathol 83: 59–68.
Kim GH, Yun HK, Choi CS, Park JH, Jung YJ, Park KS, Dane F, Kang KK (2008). Identification of AFLP and RAPD markers linked to anthracnose resistance in grapes and their conversion to SCAR markers. Plant Breeding 127: 418–423.
Kobe B, Deisenhofer J (1994). The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19: 415–421.
Kong X, Lv W, Jiang S, Zhang D, Cai G, Pan J, Li D (2013). Genomewide identification and expression analysis of calciumdependent protein kinase in maize. BMC Genomics 14: 433.
Kono A, Nakaune R, Yamada M, Nakano M, Mitani N, Ueno T (2009). Effect of culture conditions on conidia formation by Elsinoe ampelina, the causal organism of grapevine anthracnose. Plant Dis 93: 481–484.
Kortekamp A, Welter L, Vogt S, Knoll A, Schwander F, Töpfer R, Zyprian E (2008). Identification, isolation and characterization of a CC-NBS-LRR candidate disease resistance gene family in grapevine. Mol Breeding 22: 421–432.
Lee DH (1962). Study on the control of ripe rot disease of grape. J Plant Protection 1: 47–50.
Letunic I, Doerks T, Bork P (2009). SMART 6: recent updates and new developments. Nucleic Acids Res 37: D229–D232 (database issue).
Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X (1997). Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479–489.
Liu J, Liu X, Dai L, Wang G (2007). Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. J Genet Genomics 34: 765–776.
Lupas A (1996). Coiled coils: new structures and new functions. Trends Biochem Sci 21: 375–382.
Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000). The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26: 403–410.
Melksham KJ, Weckert MA, Steel CC (2002). An unusual bunch rot of grapes in sub-tropical regions of Australia caused by Colletotrichum acutatum. Australas Plant Path 31: 193–194.
Metraux JP (2001). Systemic acquired resistance and salicylic acid: current state of knowledge. Eur J Plant Pathol 107: 13–18.
Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND (1999). Plant disease resistance genes encode members of an ancient and diverse protein family with in the nucleotide-binding superfamily. Plant J 20: 317–332.
Meyers BC, Kozik A, Griego A, Kuang HH, Michelmore RW (2003). Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15: 809–834.
Meyers BC, Morgante M, Michelmore RW (2002). TIR-X and TIRNBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J 32: 77–92.
Monosi B, Wisser RJ, Penill L, Hulbert SH (2004). Full-genome analysis of resistance gene homologues in rice. Theor Appl Genet 109: 1434–1447.
Morel J, Dangl JL (1997). The hypersensitive response and the induction of cell death in plants. Cell Death Differ 4: 671–683.
Nooren IMA, Kaptein R, Sauer RT, Boelens R (1999). The tetramerization domain of the Mnt repressor consists of two right handed coiled coils. Nat Struct Biol 6: 755–759.
Pan Q, Wendel J, Fluhr R (2000). Divergent evolution of plant NBSLRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 50: 203–213.
Qi D, DeYoung BJ, Innes RW (2012). Structure-function analysis of the coiled-coil and leucine-rich repeat domains of the RPS5 disease resistance protein. Plant Physiol 158: 1819–1832.
Reisch BI, Owens CL, Cousins PS (2012). Grape. In: Badenes ML, Byrne DH, editors. Fruit Breeding; Handbook of Plant Breeding (II). New York, NY, USA: Springer, pp. 225–262.
Saitou N, Nei M (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.
Saraste M, Sibbald PR, Wittinghofer A (1990). The P-loop—a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci 15: 430–434.
Sharmin S, Moosa MM, Islam MS, Kabir I, Akter A, Khan H (2011). Identification of a novel dehydration responsive transcript from tossa jute (Corchorus olitirius L.). J Cell Mol Biol 9: 21–29.
Shirasu K, Schulze-Lefert P (2003). Complex formation, promiscuity and multi-functionality: protein interactions in diseaseresistance pathways. Trends Plant Sci 8: 252–258.
Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JDG (1995). Molecular genetics of plant disease resistance. Science 268: 661–667.
Taler D, Galperin M, Benjamin I, Cohen Y, Kenigsbuch D (2004). Plant R genes that encode photorespiratory enzyme confer resistance against disease. Plant Cell 16: 172–184.
Tameling WIL, Elzinga SDJ, Darmin PS, Vossen JH, Takken FLW, Haring MA, Cornelissen BJC (2002). The tomato R gene products I-2 and Mi-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14: 2929–2939.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30: 2725–2729.
Tan X, Meyers BC, Kozik A, West MA, Morgante M, St Clair DA, Bent AF, Michelmore RW (2007). Global expression analysis of nucleotide binding site-leucine rich repeat-encoding and related genes in Arabidopsis. BMC Plant Biol 7: 56.
Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Katagiri F (2003). Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15: 317–330.
Traut TW (1994). The function and consensus motifs of nine types of peptide segments that form different types of nucleotidebinding sites. Eur J Biochem 222: 9–19.
Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, Fitzgerald LM, Vezzulli S, Reid J et al. (2007). A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2: E1326.
Wang Q, Zhang Y, Gao M, Jiao C, Wang X (2011). Identification and expression analysis of a pathogen responsive PR-1 gene from Chinese wild Vitis quinquangularis. Afr J Biotechnol 10: 17062–17069.
Warren RF, Henk A, Mowery P, Holub E, Innes RW (1998). A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell 10: 1439–1452.
Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang Z, Kono I, Kurata N, Yano M, Iwata N, Sasaki T (1998). Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterialinoculation. P Natl Acad Sci USA 95: 1663–1668.
Yun HK, Park KS, Roh JH, Choi YJ, Jeong SB (2007). Developing a screening system for resistance to anthracnose in grapevines using culture filtrates from Elsinoe ampelina. J Hortic Sci Biotech 82: 360–364.
Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D (2004). Genome-wide identification of NBS genes in Japonica rice reveals significant expansion of divergent non-TIR NBSLRR genes. Mol Genet Genomics 271: 402–415.