Please wait a minute...
Journal of Integrative Agriculture  2011, Vol. 10 Issue (6): 827-837    DOI: 10.1016/S1671-2927(11)60068-0
Advanced Online Publication | Current Issue | Archive | Adv Search |
Natural Variation of Pto and Fen Genes and Marker-Assisted Selection for Resistance to Bacterial Speck in Tomato
SUN Wan-yu, ZHAO Wan-ying, WANG Yuan-yuan, PEI Cheng-cheng and YANG Wen-cai
Department of Vegetable Science, College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  The resistance in tomato plants to bacterial speck caused by Pseudomonas syringae pv. tomato is triggered by the interactions between the plant resistance protein Pto and the pathogen avirulence proteins AvrPto or AvrPtoB. Fen is a gene encoding closely related functional protein kinases as the Pto gene. To investigate the status of resistance to the pathogen and natural variation of Pto and Fen genes in tomato, 67 lines including 29 growing in China were subject to disease resistance evaluation and fenthion-sensitivity test. Alleles of Pto and Fen were amplified from genomic DNA of 25 tomato lines using polymerase chain reaction (PCR) and sequences were determined by sequencing the PCR products. The results indicated that none of the 29 cultivars/hybrids growing in China were resistant to bacterial speck race 0 strain DC3000. Seven of eight tomato lines resistant to DC3000 were also fenthion-sensitive. Analysis of deduced amino acid sequences identified three novel residue substitutions between Pto and pto, and one new substitution identified between Fen and fen. A PCR-based marker was developed and successfully used to select plants with resistance to DC3000.

Abstract  The resistance in tomato plants to bacterial speck caused by Pseudomonas syringae pv. tomato is triggered by the interactions between the plant resistance protein Pto and the pathogen avirulence proteins AvrPto or AvrPtoB. Fen is a gene encoding closely related functional protein kinases as the Pto gene. To investigate the status of resistance to the pathogen and natural variation of Pto and Fen genes in tomato, 67 lines including 29 growing in China were subject to disease resistance evaluation and fenthion-sensitivity test. Alleles of Pto and Fen were amplified from genomic DNA of 25 tomato lines using polymerase chain reaction (PCR) and sequences were determined by sequencing the PCR products. The results indicated that none of the 29 cultivars/hybrids growing in China were resistant to bacterial speck race 0 strain DC3000. Seven of eight tomato lines resistant to DC3000 were also fenthion-sensitive. Analysis of deduced amino acid sequences identified three novel residue substitutions between Pto and pto, and one new substitution identified between Fen and fen. A PCR-based marker was developed and successfully used to select plants with resistance to DC3000.
Keywords:  tomato      bacterial speck      Pto      Fen      natural variation      marker-assisted selection  
Received: 10 June 2011   Accepted: Online: 10 June 2011  
Corresponding Authors:  YANG Wen-cai   
About author:  SUN Wan-yu, E-mail: wanyu-920@163.com; Correspondence YANG Wen-cai, Professor, Tel: +86-10-62734136, E-mail: yangwencai@cau.edu.cn

Cite this article: 

SUN Wan-yu, ZHAO Wan-ying, WANG Yuan-yuan, PEI Cheng-cheng and YANG Wen-cai. 2011. Natural Variation of Pto and Fen Genes and Marker-Assisted Selection for Resistance to Bacterial Speck in Tomato. Journal of Integrative Agriculture, 10(6): 827-837.

Arredondo C R, Davis R M. 2000. First report of Pseudomonas syringae pv. tomato race 1 on tomato in California. Plant Disease, 84, 371.

Buonaurio R, Stravato V M, Cappelli C. 1996. Occurrence of Pseudomonas syringae pv. tomato race 1 in Italy on Pto gene-bearing tomato plants. Journal of Phytopathology, 144, 437-440.

Carland F M, Staskawicz B J. 1993. Genetic characterization of the Pro locus of tomato: semi-dominance and cosegregation of resistance to Pseudomonas syringae pathovar tomato and sensitivity to the insecticide Fenthion. Molecular and General Genetics, 239, 17-27.

Chang J H, Tai Y S, Bernal A J, Lavelle D T, Staskawicz B J,Michelmore R W. 2002. Functional analyses of the Pto resistance gene family in tomato and the identification of a minor resistance determinant in a susceptible haplotype.Molecular Plant-Microbe Interactions, 15, 281-291.

Chen J, Wang H, Shen H L, Chai M, Li J S, Qi M F, Yang W C. 2009. Genetic variation in tomato populations from four breeding programs revealed by single nucleotide polymorphism and simple sequence repeat markers. Scientia Horticulturae, 122, 6-16.

Coaker G L, Francis D M. 2004. Mapping, genetic effects, and epistatic interaction of two bacterial canker resistance QTLs from Lycopersicon hirsutum. Theoretical and Applied Genetics, 108, 1047-1055.

Deng G, Qu X, Chen X R, Yang C D, Xue L. 2008. Pathogen identification of bacterial leaf speck of tomato based on 16S rDNA, physiology and biochemistry in Gansu Province. Plant Protection, 34, 47-51. (in Chinese)

Donner S C, Barker S J. 1996. Pto resistance will not be effective in Australia (Abstr.). In: Proceedings of the 8th International Congress on Molecular Plant-Microbe Interactions. Knoxville, TN, USA.

Emmatty D A, Scott M D, George B F. 1982. Inoculation technique to screen for bacterial speck resistance of tomatoes. Plant Disease, 66, 993-994.

Feng L Y, Zhao T C, Sun F Z, Liu Q, Wang Y S. 2000. Occurrence of tomato bacterial speck in Liaoning Province. Liaoning Agricultural Sciences, 1, 53-54. (in Chinese)

Hofmann N R. 2009. The tomato Pto kinase uses shared and unique surfaces to recognize divergent avirulence proteins.The Plant Cell, 21, 1623.

Jia Y L, Loh Y T, Zhou J M, Martin G B. 1997. Alleles of Pto and Fen occur in bacterial speck-susceptible and fenthioninsensitive tomato cultivars and encode active protein kinases.The Plant Cell, 9, 61-73.

Kabelka E, Franchino B, Francis D M. 2002. Two loci from Lycopersicon hirsutum LA407 confer resistance to strains of Clavibacter michiganensis subsp. michiganensis.Phytopathology, 92, 504-510.

Kim Y J, Lin N C, Martin G B. 2002. Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell, 109, 589-598.

King E O, Ward M K, Raney D E. 1954. Two simple media for the demonstration of pyocyanin and fluorescin. The Journal of Laboratory and Clinical Medicine, 44, 301-307.

Laterrot H, Moretti A. 1989. Linkage between Pto and susceptibility to fenthion. Report of Tomato Genetics Cooperative, 39, 21-22.

Lawton M B, MacNeill B H. 1986. Occurrence of race 1 of Pseudomonas syringae pv. tomato on field tomato in southwestern Ontario. Candian Journal of Plant Pathology, 8, 85-88.

Loh Y T, Martin G B. 1995. The disease-resistance gene Pto and the fenthion-sensitivity gene Fen encode closely related functional protein kinases. Proceedings of National Academy of Sciences of the USA, 92, 4181-4184.

Martin G B, Brommonschenkel S H, Chunwongse J, Frary A, Ganal M W, Spivey R, Wu T, Earle E D, Tanksley S D. 1993a. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science, 262, 1432-1436.

Martin G B, Carmen de Vicente M, Tanksley S D. 1993b. Highresolution linkage analysis and physical characterization of the Pto bacterial resistance locus in tomato. Molecular Plant-Microbe Interactions, 6, 26-34.

Martin G B, Frary A, Wu T, Brommonschenkel S, Chunwongse J, Earle E D, Tanksley S D. 1994. A member of the tomato Pto gene family confers sensitivity to fenthion resulting in rapid cell death. The Plant Cell, 6, 1543-1552.

Mur L A J, Kenton P, Lloyd A J, Ougham H, Prats E. 2008. The hypersensitive response; the centenary is upon us but how much do we know? Journal of Experimental Botany, 59, 501-520.

Pitblado R E, MacNeill B H. 1983. Genetic basis of resistance to Pseudomonas syringae pv. tomato in field tomatoes. Canadian Journal of Plant Pathology, 5, 251-255.

Rathjen J P, Chang J H, Staskawicz B J, Michelmore R W. 1999.Constitutively active Pto induces a Prf-dependent hypersensitive response in the absence of avrPto. EMBO Journal, 18, 3232-3240.

Rose L E, Langley C H, Bernal A J, Michelmore R W. 2005. Natural variation in the Pto pathogen resistance gene within species of wild tomato (Lycopersicon). I. Functional analysis Natural Variation of Pto and Fen Genes and Marker-Assisted Selection for Resistance to Bacterial Speck in Tomato 837 of Pto alleles. Genetics, 171, 345-357.

Rose L E, Michelmore R W, Langley C H. 2007. Natural variation in the Pto disease resistance gene within species of wild tomato (Lycopersicon). II. Population genetics of Pto. Genetics, 175,1307-1319.

Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Molecular Biology, 132, 365-386.

Sessa G, D’Ascenzo M, Martin G B. 2000. Thr-38 and Ser-198 are Pto autophosphorylation sites required for the AvrPto-Ptomediated hypersensitive response. EMBO Journal, 19, 2257-2269.

Tanksley S D, Brommonschenkel S, Martin G. 1996. Ptoh, an allele of Pto conferring resistance to Pseudomonas syringae pv. tomato (race 0) that is not associated with fenthion sensitivity. Report of Tomato Genetics Cooperative, 46, 28-29.

Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, Higgins D G. 1997. The CLUSTER_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876-4882.

Wang X H, Li G Y, Ren Y Z, Xue X W, Huang S F. 2006a.Pathogen identification of bacterial spot of processing tomato in Xinjiang. Acta Agriculturae Boreali-occidentalis Sinica,15,72-74. (in Chinese)

Wang X H, Li G Y, Ren Y Z, Xue X W, Huang S F. 2006b. Identified the resistance of processing tomato varieties to bacterial spot. Northern Horticulture, 3, 5-6. (in Chinese)

Wu A J, Andriotis V M E, Durrant M C, Rathjen J P. 2004. A patch of surface-exposed residues mediates negative regulation of immune signaling by tomato Pto kinase. The Plant Cell,16, 2809-2821.

Yang W C, Francis D M. 2005. Marker-assisted selection for combining resistance to bacterial spot and bacterial speck in tomato. Journal of the American Society for Horticultural Science, 130, 716-721.

Yang W C, Francis D M. 2007. Genetics and breeding for resistance to bacterial diseases in tomato: prospects for marker assisted selection. In: Razdan M K, Mattoo A K, eds., Genetic Improvement of Solanaceous Crops. vol. 2: Tomato. Science Publishers, USA. pp. 379-420.

Zhao T C, Sun F Z, Feng L Y, Han W H, Xu W K. 2000.Evaluation of resistance to bacterial speck in tomato. Plant Protection, 26, 49-50. (in Chinese)

Zhao T C, Sun F Z, Li M Y, Zhang G F, Dai C Z, Cui Y Y, Yang H, Wang W L. 2004. Occurrence and control of bacterial speck in tomato. China Vegetables, 4, 64. (in Chinese)

Zhao T C, Sun F Z, Song W S. 2001a. Pathogen identification of bacterial speck of tomato. Acta Phytopathologica Sinica, 31,37-42. (in Chinese)

Zhao T C, Yu L, Sun F Z, Feng L Y. 1999. Occurrence and control of tomato bacterial speck. Plant Protection, 25, 56.(in Chinese)

Zhao Z J, Lin Z M, Zhao X J, Zhao T C, Sun F Z. 2001b.Occurrence of tomato bacterial speck in Shanxi Province.Plant Protection Technology and Extension, 21, 37. (in Chinese)
[1] Xuehao Zhang, Qiuling Zheng, Yongjiang Hao, Yingying Zhang, Weijie Gu, Zhihao Deng, Penghui Zhou, Yulin Fang, Keqin Chen, Kekun Zhang. Physiology and transcriptome profiling reveal the drought tolerance of five grape varieties under high temperatures[J]. >Journal of Integrative Agriculture, 2025, 24(8): 3055-3072.
[2] Jiazhi Sun, Bingyun Yang, Lingmin Xia, Rui Yang, Chaoyang Ding, Yang Sun, Xing Chen, Chunyan Gu, Xue Yang, Yu Chen. Amino acid substitutions in succinate dehydrogenase complex conferring resistance to the SDHI fungicide pydiflumetofen in Cochliobolus heterostrophus causing southern corn leaf blight[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2670-2685.
[3] Wei Wang, Chuxiao Lin, Yirong Zhang, Shiyan Liu, Jiali Liu, Xinnian Zeng. Four signal chemicals can non-destructively induce enhanced resistance to Asian citrus psyllids in Citrus sinensis while maintaining balanced plant growth and development[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2732-2748.
[4] Lifang Yuan, Hang Jiang, Qibao Liu, Xilong Jiang, Yanfeng Wei, Xiangtian Yin, Tinggang Li. Acidic environment favors the development and pathogenicity of the grape white rot fungus Coniella vitis[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2686-2703.
[5] Shudong Chen, Yupan Zou, Xin Tong, Cao Xu. A tomato NBS-LRR gene Mi-9 confers heat-stable resistance to root-knot nematodes[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2869-2875.
[6] Xinyi Mao, Xuan Zhao, Zhi Luo, Ao He, Meng Yang, Mengjun Liu, Jin Zhao, Ping Liu. Transcriptome-based analysis of lignin accumulation in the regulation of fruit stone development and endocarp hardening in Chinese jujube[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2217-2228.
[7] Jiaying Ma, Jian Liu, Yue Wen, Zhanli Ma, Jinzhu Zhang, Feihu Yin, Tehseen Javed, Jihong Zhang, Zhenhua Wang. Enhancing the yield and water use efficiency of processing tomatoes (Lycopersicon esculentum Miller) through optimal irrigation and salinity management under mulched drip irrigation[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2410-2424.
[8] Shan Wang, Kailin Shi, Yufan Xiao, Wei Ma, Yiguo Hong, Daling Feng, Jianjun Zhao. The circadian clock shapes diurnal gene expression patterns linked to glucose metabolic processes in Chinese cabbage[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2155-2170.
[9] Teame Gereziher Mehari, Marijana Skorić, Hui Fang, Kai Wang, Fang Liu, Tesfay Araya, Branislav Šiler, Dengbing Yao, Baohua Wang. Insights into the role of GhCYP and GhTPS in the gossypol biosynthesis pathway via a multiomics and functional-based approach in cotton[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1671-1687.
[10] Xuemei Hou, Meimei Shi, Zhuohui Zhang, Yandong Yao, Yihua Li, Changxia Li, Wenjin Yu, Chunlei Wang, Weibiao Liao. DNA demethylation is involved in nitric oxide-induced flowering in tomato[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1769-1785.
[11] Congrui Sun, Runze Wang, Jiaming Li, Xiaolong Li, Bobo Song, David Edwards, Jun Wu. Pan-transcriptome analysis provides insights into resistance and fruit quality breeding of pear (Pyrus pyrifolia)[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1813-1830.
[12] Jin Wang, Minghua Wei, Haiyan Wang, Changjuan Mo, Yingchun Zhu, Qiusheng Kong. A time-course transcriptome reveals the response of watermelon to low-temperature stress[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1786-1799.
[13] Qibing Gu, Xiayu Zhu, Qiankun Bai, Chengyuan Ji, Yue Zhang, Jiale Ma, Huochun Yao, Zihao Pan. Bioinformatics analysis of type II toxin–antitoxin systems and regulatory functional assessment of HigBA and SS-ATA in Streptococcus suis[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1958-1971.
[14] Bin Li, Wangpeng Shi, Shaoqun Zhou, Guirong Wang. Oral secretions: A key molecular interface of plant–insect herbivore interactions[J]. >Journal of Integrative Agriculture, 2025, 24(4): 1342-1358.
[15] Ru Bao, Tianli Guo, Zehua Yang, Chengyu Feng, Junyao Wu, Xiaomin Fu, Liu Hu, Changhai Liu, Fengwang Ma. Overexpression of the apple m6A demethylase gene MdALKBH1A regulates resistance to heat stress and fixed-carbon starvation[J]. >Journal of Integrative Agriculture, 2025, 24(4): 1489-1502.
No Suggested Reading articles found!