AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (14.5 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research paper

Molecular cloning and functional analysis of the pepper resistance gene Me3 to root-knot nematode

Yang Liu1Hongyi Cao1Jian LingYuhong YangYan LiBingyan XieJianlong Zhao( )Zhenchuan Mao( )
Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing 100081, China

1 These authors contributed equally to this work. Peer review under responsibility of Chinese Society of Horticultural Science (CSHS) and Institute of Vegetables and Flowers (IVF), Chinese Academy of Agricultural Sciences (CAAS)

Show Author Information

Abstract

Root-knot nematodes (RKNs) cause severe diseases in peppers annually around the world. In pepper, the Me3 gene provides a heat-stable and broad-spectrum resistance to RKNs. In this study, several simple sequence repeat (SSR) markers and insertion/deletion (InDel) markers were developed to fine map the Me3 gene. Analysis of 2272 individuals (F2 progenies) revealed that Me3 was located in a 45-kb DNA region between markers SSR784 and SSR339, in which there were three candidate genes. Among them, as a novel nucleotide binding site and leucine rich repeat (NBS-LRR) family gene, the DNA sequence of Capana09g000163 of pepper line 'HDA149' was 6348 bp in length, with a 2802-bp open reading frame encoding 933 amino acids, including NB-ARC and LRR domains. Tobacco transient expression assays demonstrated that expression of Capana09g000163 triggered a hypersensitive response (HR) in Nicotiana benthamiana leaves. Subcellular localization results showed that the Capana09g000163 protein was localized in the cell nucleus. Ectopic expression of Capana09g000163 in Arabidopsis significantly increased resistance against Meloidogyne incognita compared with the wild-type (WT) Arabidopsis. Furthermore, M. incognita was almost unable to develop in transgenic Arabidopsis expressing Capana09g000163. Taken together, we cloned the Me3 gene and verified that it induced resistance against M. incognita with the methods of map-based cloning and transgenic technology, which may be of great significance to pepper breeding for resistance against RKNs.

References

 

Abdul, M.K., Asif, A.K., Muhammad, T.A., Luqman, A., Hafiza, M.N.C., 2015. Comparative analysis of resistance gene analogues encoding NBS-LRR domains in cotton. J Sci Food Agric, 96: 530-538.

 

Albert, V.A., Chang, T.H., 2014. Evolution of a hot genome. P Natl A Sci, 111: 5069-5070.

 

Bleve-Zaccheo, T., Bongiovanni, M., Melillo, M.T., Castagnone-Sereno, P., 1998. The pepper resistance genes Me1 and Me3 induce penetration rates and temporal sequences of root cell ultrastructural changes upon nematode infection. Plant Sci, 133: 79-90.

 

Bucki, P., Paran, I., Ganot, L., Ozalvo, R., Iberkleid, I., Miyara, S.B., 2017. Pathogenic variability of Meloidogyne incognita populations occurring in pepper-production greenhouses in Israel toward Me1, Me3 and N pepper resistance genes. Plant Dis, 101: 1391-1401.

 

Celik, I., Sogut, M.A., Ozkaynak, E., Doganlar, S., Frary, A., 2016. Physical mapping of NBS-coding resistance genes to the Me gene cluster on chromosome P9 reveals markers tightly linked to the N gene for root-knot nematode resistance in pepper. Mol Breed, 36: 137.

 

Changkwian, A., Venkatesh, J., Lee, J.H., Han, J.W., Kwon, J.K., Siddique, M.I., Solomon, A.M., Choi, G.J., Kim, E., Seo, Y., 2019. Physical localization of the root-knot nematode (Meloidogyne incognita) resistance locus Me7 in pepper (Capsicum annuum). Front Plant Sci, 10: 886.

 

Chen, R., Li, H., Zhang, L., Zhang, J., Xiao, J., Ye, Z., 2007. Cami, a root-knot nematode resistance gene from hot pepper (Capsium annuum L.) confers nematode resistance in tomato. Plant Cell Rep, 26: 895-905.

 

Collange, B., Navarrete, M., Peyre, G., Mateill, T., 2011. Root-knot nematode (Meloidogyne) management in vegetable crop production: the challenge of an agronomic system analysis. Crop Prot, 30: 1251-1262.

 

Djian-Caporalino, C., Fazari, A., Arguel, M.J., Vernie, T., VandeCasteele, C., Faure, I., Brunoud, G., Pijarowski, L., Palloix, A., Lefebvre, V., Abad, P., 2007. Root-knot nematode (Meloidogyne spp.) Me resistance genes in pepper (Capsicum annuum L.) are clustered on the P9 chromosome. Theor Appl Genet, 114: 473-486.

 

Djian-Caporalino, C., Palloix, A., Fazari, A., Marteu, N., Barbary, A., Abad, P., 2014. Pyramiding, alternating or mixing: comparative performances of deployment strategies of nematode resistance genes to promote plant resistance efficiency and durability. BMC Plant Biol, 14: 53-56.

 

Djian-Caporalino, C., Pijarowski, L., Fazari, A., Samson, M., Gaveau, L., O'Byrne, C., Lefebvre, V., Caranta, C., Palloix, A., Abad, P., 2001. High-resolution genetic mapping of the pepper (Capsicum annuum L.) resistance loci Me3 and Me4 conferring heat-stable resistance to root-knot nematodes (Meloidogyne spp.). Theor Appl Genet, 103: 592-600.

 

Djian-Caporalino, C., Pijarowski, L., Januel, A., Lefebvre, V., Daubeze, A., Palloix, A., 1999. Spectrum of resistance to root-knot nematodes and inheritance of heat-stable resistance in pepper (Capsicum annuum L.). Theor Appl Genet, 99: 496-502.

 

Ernst, K., Kumar, A., Kriseleit, D., Kloos, D.U., Phillips, M.S., Ganal, M.W., 2002. The broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J, 31: 127-136.

 

Fazari, A., Palloix, A., Wang, L., Hua, M.Y., Sage-Palloix, A.M., Zhang, B.X., Djian-Caporalino, C., 2012. The root-knot nematode resistance N-gene co-localizes in the Me-genes cluster on the pepper (Capsicum annuum L.) P9 chromosome. Plant Breed, 131: 665-673.

 

Fery, R.L., Dukes, P.D., 1996. The inheritance of resistance to the southern root-knot nematode in 'Carolina Hot' cayenne pepper. J Am Soc Hortic Sci, 121: 1024-1027.

 

Fery, R.L., Dukes, P.D., Thies, J.A., 1998. 'Carolina Wonder' and 'Charleston Belle': southern root knot nematode-resistant bell peppers. Hortscience, 33: 900-902.

 

Guo, G.J., Wang, S.B., Liu, J.B., Pan, B.G., Diao, W.P., Ge, W., Gao, C.Z., John, C.S., 2017. Rapid identification of QTLs underlying resistance to cucumber mosaic virus in pepper (Capsicum frutescens). Theor Appl Genet, 130: 41-52.

 

Hare, W.W., 1957. Inheritance of resistance to root-knot nematodes in pepper. Phytopathology, 47: 455-459.

 

Hendy, H., Dalmasso, A., Cardin, C., 1985. Differences inresistant Capsicum annuum attacked by different Meloidogyne species. Nematologica, 31: 72-78.

 

Hiroki, T., Akira, A., Kentaro, Y., Shunichi, K., Satoshi, N., Chikako, M., Aiko, U., Hiroe, U., Muluneh, T., Shohei, T., Hideki, I., Liliana, M.C., Sophien, K., Ryohei, T., 2013. QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J, 74: 174-179.

 

Huang, S.W., Zhang, B.X., Dan, M., Linda, C., Yang, G.M., Guo, J.Z., 2000. Development of pepper SSR markers from sequence databases. Euphytica, 117: 163-167.

 

Hwang, C.F., Bhakta, A.V., Truesdell, G.M., Pudlo, W.M., Williamson, V.M., 2000. Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell, 12: 1319-1329.

 

Jesse, T., Wijbrandi, J., Heinen, L., Hogers, R., Frijters, A., Groenendijk, J., Diergaarde, P., Reijans, M., Hontelez, J., 1998. The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat Biotech, 16: 1365-1369.

 

Judy, A.T., Jennifer, J.A., 2009. Comparison between the N and Me3 genes conferring resistance to the root-knot nematode (Meloidogyne incognita) in genetically different pepper lines (Capsicum annuum). Eur J Plant Pathol, 125: 545-550.

 

Kim, S., Park, M., Yeom, S.I., Kim, Y.M., Lee, J.M., Lee, H.A., Seo, E., Choi, J., Cheong, K., Kim, K.T., Jung, K., Lee, G.W., Oh, S.K., Bae, C., Kim, S.B., Lee, H.Y., Kim, S.Y., Kim, M.S., Kang, B.C., Jo, Y.D., Yang, H.B., Jeong, H.J., Kang, W.H., Kwon, J.K., Shin, C., Lim, J.Y., Park, J.H., Huh, J.H., Kim, J.S., Kim, B.D., Cohen, O., Paran, I., Suh, M.C., Lee, S.B., Kim, Y.K., Shin, Y., Noh, S.J., Park, J., Seo, Y.S., Kwon, S.Y., Kim, H.A., Park, J.M., Kim, H.J., Choi, S.B., Bosland, P.W., Reeves, G., Jo, S.H., Lee, B.W., Cho, H.T., Choi, H.S., Lee, M.S., Yu, Y., Do Choi, Y., Park, B.S., Van Deynze, A., Ashrafi, H., Hill, T., Kim, W.T., Pai, H.S., Ahn, H.K., Yeam, I., Giovannoni, J.J., Rose, J.K.C., Sorensen, I., Lee, S.J., Kim, R.W., Choi, I.Y., Choi, B.S., Lim, J.S., Lee, Y.H., Choi, D., 2014. Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat Genet, 46: 270-278.

 

Kosambi, D.D., 2011. The estimation of map distances from recombination values. Ann Hum Genet, 12: 172-175.

 

Li, H., Durbin, R., 2009. Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics, 25: 1754-1760.

 

Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., 2009. The Sequence alignment/map (SAM) format and SAMtools. Bioinformatics, 25: 2078-2079.

 

Li, W.P., Cheng, J.W., Wu, Z.M., Qin, C., Tan, S., Tang, X., Cui, J.J., Zhang, L., Hu, K.L., 2015. An InDel-based linkage map of hot pepper (Capsicum annuum). Mol Breed, 35: 32.

 

Liu, J., Yang, H., Fei, B., Ao, K., Zhang, X., Zhang, Y., Yang, S., Gitta, C., 2015. IBR5 modulates temperature-dependent, R protein CHS3-mediated defense responses in Arabidopsis. PLoS Genet, 11: 1-24.

 

Livak, K.J., Schmittgen, T.D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 25: 402-408.

 

Lu, H., Lin, T., Klein, J., Wang, S., Qi, J., Zhou, Q., Sun, J., Zhang, Z., Weng, Y., Huang, S., 2014. QTL-seq identifies an early flowering QTL located near flowering locus T in cucumber. Theor Appl Genet, 127: 1491-1499.

 

Mao, Z.C., Zhu, P.P., Liu, F., Huang, Y.H., Ling, J., Chen, G.H., Yang, Y.H., Feng, D.X., Xie, B.Y., 2015. Cloning and functional analyses of pepper CaRKNR involved in Meloidogyne incognita resistance. Euphytica, 205: 903-913.

 

Michelmore, R.W., Paran, I., Kesseli, R.V., 1991. Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. P Natl Acad Sci USA, 88: 9828-9832.

 

Milligan, S.B., Bodeau, J., Yaghoobi, J., Kaloshian, I., Zabel, P., Williamson, V.M., 1998. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell, 10: 1307-1319.

 

Min, J., Sun, H.S., Jeon, E.M., Park, J.M., Harn, C.H., 2015. Pepper, chili (Capsicum annuum). Methods Mol Biol, 1223: 311-320.

 

Murray, M.G., Thompson, W.F., 1980. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res, 8: 4321-4325.

 

Paal, J., Henselewski, H., Muth, J., Meksem, K., Menéndez, C.M., Salamini, F., Ballvora, A., Gebhardt, C., 2004. Molecular cloning of the potato Gro 1-4 gene conferring resistance to pathotype Ro1 of the root cyst nematode Globodera rostochiensis, based on a candidate gene approach. Plant J, 38: 85-297.

 

Pal, A., Chakrabarti, A., Basak, J., 2007. New motifs within the NB-ARC domain of R proteins: probable mechanisms of integration of geminiviral signatures within the host species of Fabaceae family and implications in conferring disease resistance. J Theor Biol, 246: 564-573.

 

Pegard, A., Brizzard, G., Fazari, A., Soucaze, O., Abad, P., Djian-Caporalino, C., 2005. Histological characterization of resistance to different root-knot nematode species related to phenolics accumulation in Capsicum annuum L. Phytopathology, 95: 158-165.

 

Qin, C., Yu, C., Shen, Y., Fang, X., Chen, L., Min, J., Cheng, J., Zhao, S., Xu, M., Luo, Y., Yang, Y., Wu, Z., Mao, L., Wu, H., Ling-Hu, C., Zhou, H., Lin, H., González-Morales, S., Trejo-Saavedra, D., Tian, H., Tang, X., Zhao, M., Huang, Z., Zhou, A., Yao, X., Cui, J., Li, W., Chen, Z., Feng, Y., Niu, Y., Bi, S., Yang, X., Li, W., Cai, H., Luo, X., Montes-Hernández, S., Leyva-González, M., Xiong, Z., He, X., Bai, L., Tan, S., Tang, X., Liu, D., Liu, J., Zhang, S., Chen, M., Zhang, L., Zhang, L., Zhang, Y., Liao, W., Zhang, Y., Wang, M., Lv, X., Wen, B., Liu, H., Luan, H., Zhang, Y., Yang, S., Wang, X., Xu, J., Li, X., Li, S., Wang, J., Palloix, A., Bosland, P., Li, Y., Krogh, A., Rivera-Bustamante, R., Herrera-Estrella, L., Yin, Y., Yu, J., Hu, K., Zhang, Z., 2014. Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization. P Natl Acad Sci USA, 111: 5135-5140.

 

Ramirez-Malagon, O.A., 2001. Invited review: in vitro chili pepper biotechnology. Vitro Cell Dev-Pl, 37: 701-729.

 

Ros, C., Lacasa, C.M., Martínez, V., Bielza, P., Lacasa, A., 2014. Response of pepper root stocks to co-infection of Meloidogyne incognita and Phytophthora spp. Eur J Hortic Sci, 79: 22-28.

 

Ros, C., Martínez, V., Sánchez-Solana, F., López-Marín, J., Lacasa, C.M., Del Mar Guerrero, M., Lacasa, A., 2018. Combination of biosolarization and grafting to control Meloidogyne incognita in greenhouse pepper crops. Crop Prot, 113: 33-39.

 
Starr, J.L., Bridge, J., Cook, R., 2002. Resistance to Plant-Parasitic Nematodes: History, Current Use and Future Potential. CABI Publishing, Wallingford, UK, pp. 1-22.
 

Uncu, A.T., Celik, I., Devran, Z., Ozkaynak, E., Frary, A., Doganlar, S., 2015. Development of a SNP-based CAPS assay for the Me1 gene conferring resistance to root knot nematodes in pepper. Euphytica, 206: 393-399.

 

Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B.C., Remm, M., Rozen, S.G., 2012. Primer 3-new capabilities and interfaces. Nucleic Acids Res, 40: 115.

 

van der Vossen, E.A., Van Der Voort, J.N., Kanyuka, K., Bendahmane, A., Sandbrink, H., Baulcombe, D.C., Bakker, J., Stiekema, W.J., Klein-Lankhorst, R.M., 2000. Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J, 23: 567-576.

 

van Ooijen, J., 2006. JoinMap 4.0, Software for the calculation of genetic linkage maps in experimental populations. Kyazma Bv, 33: 145-148.

 
Wang, G.L., Zhang, F.L., Cai, W.Q., Chen, X., Shang, H.S., 2002. Virusresistant Chili Pepper Produced by Agrobacterium Species-Mediated Transformation. M-Publishing Inc., New York, pp. 563-578.
 

Wang, L., Gu, X., Hua, M., Mao, S., Zhang, Z., Peng, D., Yun, X., Zhang, B., 2009. A SCAR marker linked to the N gene for resistance to root knot nematodes (Meloidogyne spp.) in pepper (Capsicum annuum L.). Sci Hortic-Amsterdam, 122: 318-322.

 

Wang, X.Y., Ariane, F., Cao, Y.C., Zhang, Z.H., Alain, P., Mao, S.L., Zhang, B.X., Djian-Caporalino, C., Wang, L.H., 2018. Fine mapping of the root-knot nematode resistance gene Me1 in pepper (Capsicum annuum L.) and development of markers tightly linked to Me1. Mol Breed, 38: 39.

 

Wang, X.Y., Shi, W.C., Wang, J.L., Gao, Z., Li, S., Wang, N.X., Shi, Q.H., 2021. Control of Southern root-knot nematodes on tomato and regulation of soil bacterial community by biofumigation with Zanthoxylum bungeanum seed. Hortic Plant J, 7: 49-58.

 

Weng, W., Luo, X.W., Yang, X., Cheng, Y.F., 2013. Research progress on root-knot nematode disease resistance breeding of Solanaceous fruit vegetable. Acta Hortic Sin, 40: 1741-1751. (in Chinese)

 

Xu, X., Lu, L., Zhu, B., Xu, Q., Qi, X., Chen, X., 2015. QTL mapping of cucumber fruit flesh thickness by SLAF-seq. Sci Rep-UK, 5: 15829.

 

Xu, X.Y., Liu, F., Kang, H.X., Zhang, Z.Q., 2011. Fine mapping of the root-knot nematode resistance gene Me3 in pepper. Acta Hortic Sin, 38: 288-294. (in Chinese)

 

Zhang, H.F., Liu, S.Y., Ma, J.H., Wang, X.K., Meng, Y.C., Zhang, Y.M., Chen, R.G., 2019. Cadhn4, a salt and cold stress-responsive dehydrin gene from pepper decreases abscisic acid sensitivity in Arabidopsis. Int J Mol Sci, 21: 32-36.

 

Zhang, W.Y., Mao, Z.C., Shen, B.M., Wang, G., Yao, Y.R., Feng, D.X., Xie, B.Y., 2014. Overexpression of pepper CaSn gene enhances resistance to Meloidogyne incognita in transgenic plants. Acta Hortic Sin, 41: 80-88. (in Chinese)

 

Zhang, X., Henriques, R., Lin, S.S., Niu, Q.W., Chua, N.H., 2006. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc, 1: 641-646.

 

Zhao, J., Mejias, J., Quentin, M., Chen, Y., De Almeida-Engler, J., Mao, Z., Sun, Q., Liu, Q., Xie, B., Abad, P., Favery, B., Jian, H., 2020. The root-knot nematode effector MiPDI1 targets a stress-associated protein (SAP) to establish disease in Solanaceae and Arabidopsis. New Phytol, 228: 1417-1430.

 

Zhao, J., Sun, Q., Quentin, M., Ling, J., Abad, P., Zhang, X., Li, Y., Yang, Y., Favery, B., Mao, Z., Xie, B., 2021. A Meloidogyne incognita C-type lectin effector targets plant catalases to promote parasitism. New Phytol, 232: 2124-2137.

Horticultural Plant Journal
Pages 133-144
Cite this article:
Liu Y, Cao H, Ling J, et al. Molecular cloning and functional analysis of the pepper resistance gene Me3 to root-knot nematode. Horticultural Plant Journal, 2023, 9(1): 133-144. https://doi.org/10.1016/j.hpj.2022.12.003

430

Views

17

Downloads

3

Crossref

2

Web of Science

7

Scopus

2

CSCD

Altmetrics

Received: 07 March 2022
Revised: 13 July 2022
Accepted: 09 October 2022
Published: 15 December 2022
© 2022 Chinese Society for Horticultural Science (CSHS) and Institute of Vegetables and Flowers (IVF), Chinese Academy of Agricultural Sciences (CAAS).

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return