Identification of Mi-1 homologs in various Solanum species
Article Sidebar
Published:
May 21, 2018
Keywords:
homologs, Meloidogyne, Mi-1 gene, resistance, Solanum
Main Article Content
Abstract
In Ecuador, several solanaceous crops, including naranjilla (Solanum quitoense), are attacked by the nematode Meloidogyne sp. Resistant cultivars are not available and there is a need to identify potential sources of resistance that can be incorporated into breeding programs. The Mi-1 gene from S. peruvianum is known to confer resistance to Meloidogyne in tomato (S. lycopersicum).
In this study, 42 plant accessions of wild and cultivated Solanum species were screened to identify the presence of this gene, its diversification, expression, and evidence of gene recombination. The Mi-1 gene (exon 3) was identified in 34 accessions. Sixteen alleles were identified, that encode 15 different amino acid sequences, all of which encode NBS-LRR proteins and share 72-96 % homology with the tomato Mi-1 protein. The Mi-1 locus was highly polymorphic; most polymorphisms tend to accumulate in the NBS rather than in the LRR region. Genetic recombination was detected among the tomato and potato relate d sequences, but it was absent in the naranjilla group. Homologs identified expressed in both non-infected roots and leaves of some accessions, suggesting the constitutive expression of the gene.
Downloads
Download data is not yet available.
Article Details
How to Cite
1.
Carrera Pacheco SE, Chacón Acosta MG, Vallejo López MJ, Jarrín Cornejo FJ, Oliva Pérez RF, Proaño KI. Identification of Mi-1 homologs in various Solanum species. REMCB [Internet]. 2018May21 [cited 2024Jul.3];39(1). Available from: https://remcb-puce.edu.ec/remcb/article/view/566
Issue
Section
Artículos Científicos
References
Ammiraju J, Veremis J, Huang X, Roberts P, Kaloshian I. 2003. The heat-stable root-knot nematode resistance gene Mi-9 from Lycopersicon peruvianum is localized on the short arm of chromosome 6. Theor. Appl. Genet. 106:478–484. doi:10.1007/s00122-002-1106-y.
Belkhadir Y, Subramaniam R, Dangl JL. 2004. Plant disease resistance protein signaling: NBS–LRR proteins and their partners. Curr. Opin. Plant Biol. 7:391–399. doi:10.1016/j.pbi.2004.05.009.
Bergelson J. 2001. Evolutionary Dynamics of Plant R-Genes. Science (80-. ). 292:2281–2285. doi:10.1126/science.1061337.
Bohs L. 2005. Major clades in Solanum based on ndhF sequence data. In: Keating, R.C., Hollowell, V.C., Croat TB, editor. A Festschrift for William G. D’Arcy: The Legacy of a Taxonomist. St. Louis, Missouri. p. 27–49.
Castagnone-Sereno P. 2002. Genetic variability of nematodes: a threat to the durability of plant resistance genes? Euphytica 124:193–199. doi:10.1023/A:1015682500495.
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. doi:10.1007/s00299-007-0304-0.
Dropkin VH. 1969a. Necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature. Phytopathology.
Dropkin VH. 1969b. Cellular Responses of Plants to Nematode Infections. Annu. Rev. Phytopathol. 7:101–122. doi:10.1146/annurev.py.07.090169.000533.
Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792–1797. doi:10.1093/nar/gkh340.
Gleason CA, Williamson VM, Seah S, Yaghoobi J, Rossi M. 2004. The nematode-resistance gene, Mi-1 , is associated with an inverted chromosomal segment in susceptible compared to resistant tomato. TAG Theor. Appl. Genet. 108:1635–1642. doi:10.1007/s00122-004-1594-z.
Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95–98. doi:citeulike-article-id:691774.
Holtzmann O. 1965. Effects of soil temperature on resistance of tomato to root-knot nematode (Meloidogyne incognita). Phytopathology 55:990–992.
Huson DH. 1998. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68–73. doi:10.1093/bioinformatics/14.1.68.
Huson DH, Bryant D. 2006. Application of Phylogenetic Networks in Evolutionary Studies. Mol. Biol. Evol. 23:254–267. doi:10.1093/molbev/msj030.
INEC. 2000. III Censo Nacional Agropecuario. Resultados Censo Nacional 2000.
INEC. 2014. Encuesta de superficie y producción agropecuaria continua. Quito-Ecuador.
Jablonska B, Ammiraju JSS, Bhattarai KK, Mantelin S, de Ilarduya OM, Roberts PA, Kaloshian I. 2006. The Mi-9 Gene from Solanum arcanum Conferring Heat-Stable Resistance to Root-Knot Nematodes Is a Homolog of Mi-1. PLANT Physiol. 143:1044–1054. doi:10.1104/pp.106.089615.
Kaloshian I, Yaghoobi J, Liharska T, Hontelez J, Hanson D, Hogan P, Jesse T, Wijbrandi J, Simons G, Vos P, et al. 1998. Genetic and physical localization of the root-knot nematode resistance locus Mi in tomato. Mol. Gen. Genet. MGG 257:376–385. doi:10.1007/s004380050660.
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi:10.1093/bioinformatics/btm404.
Leipe DD, Koonin E V., Aravind L. 2004. STAND, a Class of P-Loop NTPases Including Animal and Plant Regulators of Programmed Cell Death: Multiple, Complex Domain Architectures, Unusual Phyletic Patterns, and Evolution by Horizontal Gene Transfer. J. Mol. Biol. 343:1–28. doi:10.1016/j.jmb.2004.08.023.
Mao Z, Xie B, Yang Y. 2008. Gen Capsicum annuum NBS-LRR root-knot nematode resistance protein mRNA, complete cds. Accesion FJ231739.1.
Meyers BC. 1998. The Major Resistance Gene Cluster in Lettuce Is Highly Duplicated and Spans Several Megabases. PLANT CELL ONLINE 10:1817–1832. doi:10.1105/tpc.10.11.1817.
Michelmore RW, Meyers BC. 1998. Clusters of Resistance Genes in Plants Evolve by Divergent Selection and a Birth-and-Death Process. Genome Res. 8:1113–1130. doi:10.1101/gr.8.11.1113.
Milligan SB. 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 ONLINE 10:1307–1320. doi:10.1105/tpc.10.8.1307.
Noel L. 1999. Pronounced Intraspecific Haplotype Divergence at the RPP5 Complex Disease Resistance Locus of Arabidopsis. PLANT CELL ONLINE 11:2099–2112. doi:10.1105/tpc.11.11.2099.
Nombela G, Williamson VM, Muñiz M. 2003. The Root-Knot Nematode Resistance Gene Mi-1.2 of Tomato Is Responsible for Resistance Against the Whitefly Bemisia tabaci. Mol. Plant-Microbe Interact. 16:645–649. doi:10.1094/MPMI.2003.16.7.645.
Ochoa J, Shiki L, Gallegos P, Viteri J, Ellis M, Williams R. 2008. Evaluación de alternativas racionales de manejo de las principales enfermedades de la naranjilla en Palora-Ecuador. Estac. Exp. St. Catalina. INIAP 12:10. doi:10.1017/CBO9781107415324.004.
Ota T, Nei M. 1994 May. Divergent evolution and evolution by the birth-and-death process in the immunoglobulin VH gene family. Mol. Biol. Evol. doi:10.1093/oxfordjournals.molbev.a040127.
Rambaut A. 2009. FigTree v1.4: Tree Figure Drawing Tool.
Revelo J, Mora E, León P, Viteri P, Valverde F, Martinez A, Fiallos J, Lima L, Guerra M. 2003. Manejo integrado de plagas para el mejoramiento de la producción sostenible de frutas en la Zona Andina. Estac. Exp. St. Catalina. INIAP:22. doi:10.1017/CBO9781107415324.004.
Revelo J, Perez E, Maila M V. 2004. Cultivo ecológico del tomate de árbol en Ecuador: Texto de consulta del estudiante. Estac. Exp. St. Catalina. INIAP 12:87. doi:10.1017/CBO9781107415324.004.
Roberts PA. 2002. Concepts and consequences of resistance. In: Plant resistance to parasitic nematodes. Wallingford: CABI. p. 23–41.
Roberts P a, May D. 1986. Meloidogyne incognita Resistance Characteristics in Tomato Genotypes Developed for Processing. J. Nematol. 18:353–358.
Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM. 1998. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. 95:9750–9754. doi:10.1073/pnas.95.17.9750.
Sanchez-Puerta MV, Masuelli RW. 2011. Evolution of nematode-resistant Mi-1 gene homologs in three species of Solanum. Mol. Genet. Genomics 285:207–218. doi:10.1007/s00438-010-0596-6.
Seah S, Telleen AC, Williamson VM. 2007. Introgressed and endogenous Mi-1 gene clusters in tomato differ by complex rearrangements in flanking sequences and show sequence exchange and diversifying selection among homologues. Theor. Appl. Genet. 114:1289–1302. doi:10.1007/s00122-007-0519-z.
Smith G. 1944. Embryo culture of a tomato species hybrid. Proc. Amer. Soc. Hort. Sci. 44:413–416. [accessed 2018 Jan 4]. http://ci.nii.ac.jp/naid/10005766339/en/.
Stamatakis A, Hoover P, Rougemont J, Renner S. 2008. A Rapid Bootstrap Algorithm for the RAxML Web Servers. Syst. Biol. 57:758–771. doi:10.1080/10635150802429642.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol. Biol. Evol. 28:2731–2739. doi:10.1093/molbev/msr121.
Trudgill DL. 1991. Resistance to and Tolerance of Plant Parasitic Nematodes in Plants. Annu. Rev. Phytopathol. 29:167–192. doi:10.1146/annurev.py.29.090191.001123.
Vásquez W, Viteri P, Martínez A, Villares M, Ayala G, Jácome R. 2011. Naranjilla (Solanum quitoense Lam.): Tecnologías para mejorar la productividad y calidad de la fruta.
Vossen EAG, Gros J, Sikkema A, Muskens M, Wouters D, Wolters P, Pereira A, Allefs S. 2005. The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homolog conferring broad-spectrum late blight resistance in potato. Plant J. 44:208–222. doi:10.1111/j.1365-313X.2005.02527.x.
Williamson V, Kumar A. 2006. Nematode resistance in plants: the battle underground. Trends Genet. 22:396–403. doi:10.1016/j.tig.2006.05.003.
Belkhadir Y, Subramaniam R, Dangl JL. 2004. Plant disease resistance protein signaling: NBS–LRR proteins and their partners. Curr. Opin. Plant Biol. 7:391–399. doi:10.1016/j.pbi.2004.05.009.
Bergelson J. 2001. Evolutionary Dynamics of Plant R-Genes. Science (80-. ). 292:2281–2285. doi:10.1126/science.1061337.
Bohs L. 2005. Major clades in Solanum based on ndhF sequence data. In: Keating, R.C., Hollowell, V.C., Croat TB, editor. A Festschrift for William G. D’Arcy: The Legacy of a Taxonomist. St. Louis, Missouri. p. 27–49.
Castagnone-Sereno P. 2002. Genetic variability of nematodes: a threat to the durability of plant resistance genes? Euphytica 124:193–199. doi:10.1023/A:1015682500495.
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. doi:10.1007/s00299-007-0304-0.
Dropkin VH. 1969a. Necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature. Phytopathology.
Dropkin VH. 1969b. Cellular Responses of Plants to Nematode Infections. Annu. Rev. Phytopathol. 7:101–122. doi:10.1146/annurev.py.07.090169.000533.
Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792–1797. doi:10.1093/nar/gkh340.
Gleason CA, Williamson VM, Seah S, Yaghoobi J, Rossi M. 2004. The nematode-resistance gene, Mi-1 , is associated with an inverted chromosomal segment in susceptible compared to resistant tomato. TAG Theor. Appl. Genet. 108:1635–1642. doi:10.1007/s00122-004-1594-z.
Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95–98. doi:citeulike-article-id:691774.
Holtzmann O. 1965. Effects of soil temperature on resistance of tomato to root-knot nematode (Meloidogyne incognita). Phytopathology 55:990–992.
Huson DH. 1998. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68–73. doi:10.1093/bioinformatics/14.1.68.
Huson DH, Bryant D. 2006. Application of Phylogenetic Networks in Evolutionary Studies. Mol. Biol. Evol. 23:254–267. doi:10.1093/molbev/msj030.
INEC. 2000. III Censo Nacional Agropecuario. Resultados Censo Nacional 2000.
INEC. 2014. Encuesta de superficie y producción agropecuaria continua. Quito-Ecuador.
Jablonska B, Ammiraju JSS, Bhattarai KK, Mantelin S, de Ilarduya OM, Roberts PA, Kaloshian I. 2006. The Mi-9 Gene from Solanum arcanum Conferring Heat-Stable Resistance to Root-Knot Nematodes Is a Homolog of Mi-1. PLANT Physiol. 143:1044–1054. doi:10.1104/pp.106.089615.
Kaloshian I, Yaghoobi J, Liharska T, Hontelez J, Hanson D, Hogan P, Jesse T, Wijbrandi J, Simons G, Vos P, et al. 1998. Genetic and physical localization of the root-knot nematode resistance locus Mi in tomato. Mol. Gen. Genet. MGG 257:376–385. doi:10.1007/s004380050660.
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi:10.1093/bioinformatics/btm404.
Leipe DD, Koonin E V., Aravind L. 2004. STAND, a Class of P-Loop NTPases Including Animal and Plant Regulators of Programmed Cell Death: Multiple, Complex Domain Architectures, Unusual Phyletic Patterns, and Evolution by Horizontal Gene Transfer. J. Mol. Biol. 343:1–28. doi:10.1016/j.jmb.2004.08.023.
Mao Z, Xie B, Yang Y. 2008. Gen Capsicum annuum NBS-LRR root-knot nematode resistance protein mRNA, complete cds. Accesion FJ231739.1.
Meyers BC. 1998. The Major Resistance Gene Cluster in Lettuce Is Highly Duplicated and Spans Several Megabases. PLANT CELL ONLINE 10:1817–1832. doi:10.1105/tpc.10.11.1817.
Michelmore RW, Meyers BC. 1998. Clusters of Resistance Genes in Plants Evolve by Divergent Selection and a Birth-and-Death Process. Genome Res. 8:1113–1130. doi:10.1101/gr.8.11.1113.
Milligan SB. 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 ONLINE 10:1307–1320. doi:10.1105/tpc.10.8.1307.
Noel L. 1999. Pronounced Intraspecific Haplotype Divergence at the RPP5 Complex Disease Resistance Locus of Arabidopsis. PLANT CELL ONLINE 11:2099–2112. doi:10.1105/tpc.11.11.2099.
Nombela G, Williamson VM, Muñiz M. 2003. The Root-Knot Nematode Resistance Gene Mi-1.2 of Tomato Is Responsible for Resistance Against the Whitefly Bemisia tabaci. Mol. Plant-Microbe Interact. 16:645–649. doi:10.1094/MPMI.2003.16.7.645.
Ochoa J, Shiki L, Gallegos P, Viteri J, Ellis M, Williams R. 2008. Evaluación de alternativas racionales de manejo de las principales enfermedades de la naranjilla en Palora-Ecuador. Estac. Exp. St. Catalina. INIAP 12:10. doi:10.1017/CBO9781107415324.004.
Ota T, Nei M. 1994 May. Divergent evolution and evolution by the birth-and-death process in the immunoglobulin VH gene family. Mol. Biol. Evol. doi:10.1093/oxfordjournals.molbev.a040127.
Rambaut A. 2009. FigTree v1.4: Tree Figure Drawing Tool.
Revelo J, Mora E, León P, Viteri P, Valverde F, Martinez A, Fiallos J, Lima L, Guerra M. 2003. Manejo integrado de plagas para el mejoramiento de la producción sostenible de frutas en la Zona Andina. Estac. Exp. St. Catalina. INIAP:22. doi:10.1017/CBO9781107415324.004.
Revelo J, Perez E, Maila M V. 2004. Cultivo ecológico del tomate de árbol en Ecuador: Texto de consulta del estudiante. Estac. Exp. St. Catalina. INIAP 12:87. doi:10.1017/CBO9781107415324.004.
Roberts PA. 2002. Concepts and consequences of resistance. In: Plant resistance to parasitic nematodes. Wallingford: CABI. p. 23–41.
Roberts P a, May D. 1986. Meloidogyne incognita Resistance Characteristics in Tomato Genotypes Developed for Processing. J. Nematol. 18:353–358.
Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM. 1998. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. 95:9750–9754. doi:10.1073/pnas.95.17.9750.
Sanchez-Puerta MV, Masuelli RW. 2011. Evolution of nematode-resistant Mi-1 gene homologs in three species of Solanum. Mol. Genet. Genomics 285:207–218. doi:10.1007/s00438-010-0596-6.
Seah S, Telleen AC, Williamson VM. 2007. Introgressed and endogenous Mi-1 gene clusters in tomato differ by complex rearrangements in flanking sequences and show sequence exchange and diversifying selection among homologues. Theor. Appl. Genet. 114:1289–1302. doi:10.1007/s00122-007-0519-z.
Smith G. 1944. Embryo culture of a tomato species hybrid. Proc. Amer. Soc. Hort. Sci. 44:413–416. [accessed 2018 Jan 4]. http://ci.nii.ac.jp/naid/10005766339/en/.
Stamatakis A, Hoover P, Rougemont J, Renner S. 2008. A Rapid Bootstrap Algorithm for the RAxML Web Servers. Syst. Biol. 57:758–771. doi:10.1080/10635150802429642.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol. Biol. Evol. 28:2731–2739. doi:10.1093/molbev/msr121.
Trudgill DL. 1991. Resistance to and Tolerance of Plant Parasitic Nematodes in Plants. Annu. Rev. Phytopathol. 29:167–192. doi:10.1146/annurev.py.29.090191.001123.
Vásquez W, Viteri P, Martínez A, Villares M, Ayala G, Jácome R. 2011. Naranjilla (Solanum quitoense Lam.): Tecnologías para mejorar la productividad y calidad de la fruta.
Vossen EAG, Gros J, Sikkema A, Muskens M, Wouters D, Wolters P, Pereira A, Allefs S. 2005. The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homolog conferring broad-spectrum late blight resistance in potato. Plant J. 44:208–222. doi:10.1111/j.1365-313X.2005.02527.x.
Williamson V, Kumar A. 2006. Nematode resistance in plants: the battle underground. Trends Genet. 22:396–403. doi:10.1016/j.tig.2006.05.003.