Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-10T11:36:43.988Z Has data issue: false hasContentIssue false

Effect of plant development (age and size) on the Mi-1-mediated resistance of tomato to whitefly Bemisia tabaci

Published online by Cambridge University Press:  11 April 2017

C.I. Rodríguez-Álvarez
Affiliation:
Department of Plant Protection, Institute for Agricultural Sciences (ICA), Spanish National Research Council (CSIC), Serrano 115 Dpdo., Madrid 28006, Spain
M. Muñiz
Affiliation:
Department of Plant Protection, Institute for Agricultural Sciences (ICA), Spanish National Research Council (CSIC), Serrano 115 Dpdo., Madrid 28006, Spain
G. Nombela*
Affiliation:
Department of Plant Protection, Institute for Agricultural Sciences (ICA), Spanish National Research Council (CSIC), Serrano 115 Dpdo., Madrid 28006, Spain
*
*Author for correspondence Phone: +1(34) 917452500 Fax: +1(34) 915640800 E-mail: gnombela@ica.csic.es

Abstract

Whitefly, Bemisia tabaci, is one of the most important pests of tomato, Solanum lycopersicum L. The Mi-1 gene mediates tomato resistance to the Middle East-Asia Minor 1 (MEAM1) and Mediterranean (MED) species of B. tabaci, three species of root-knot nematodes, Meloidogyne spp., and the potato aphid, Macrosiphum euphorbiae. Tomato seedlings bearing the Mi-1 gene are resistant to nematodes soon after germination but resistance to aphids is developmentally regulated; a reliable conclusion about Mi-1 resistance to B. tabaci was not available to date. In the present work, 3-, 5- and 8-week-old plants of the tomato cultivars Motelle and Moneymaker (bearing and lacking the Mi-1 gene, respectively) were simultaneously tested under free-choice (antixenosis) and no-choice (antibiosis) conditions, to assess the real influence of plant age on the Mi-1-mediated resistance to the MED species of B. tabaci. Subsequently, plants of the same age but with different level of development were compared to check whether the plant size can also affect this tomato resistance. Obtained results demonstrated that Mi-1-mediated resistance to B. tabaci is developmentally regulated, as variations in the age of bearing-Mi-1 plants affects most infestation parameters tested. Differences between cultivars with and without the Mi-1 gene were significant for 8- but not for 3-week-old plants. For 5-week-old plants, differences between cultivars were less pronounced than in older plants, expressing an intermediate level of resistance in Motelle. Plant size also influenced whitefly infestation and reproductive activity on the resistant cultivar. However, plant age has more impact than plant size on the Mi-1-mediated resistance of tomato to B. tabaci.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bas, N., Mollema, C. & Lindhout, P. (1992) Resistance in Lycopersicon hirsutum f. glabratum to the greenhouse whitefly (Trialeurodes vaporariorum) increases with plant age. Euphytica 64, 189195.Google Scholar
Birch, L.C. (1948) The intrinsic rate of natural increase of an insect population. Journal of Animal Ecology 17, 1526.Google Scholar
Boege, K. & Marquis, R.J. (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology and Evolution 20, 441448.Google Scholar
Bonato, O., Lurette, A., Vidal, C. & Fargues, J. (2007) Modelling temperature-dependent bionomics of Bemisia tabaci (Q-biotype). Physiological Entomology 32, 5055.Google Scholar
Cao, Y., Ding, X., Cai, M., Zhao, J., Lin, Y., Li, X., Xu, C. & Wang, S. (2007) The expression pattern of a rice disease resistance gene Xa3/Xa26 is differentially regulated by the genetic backgrounds and developmental stages that influence its function. Genetics 177, 523533.Google Scholar
Carmona, D., Lajeunesse, M.J. & Johnson, M.T.J. (2011) Plant traits that predict resistance to herbivores. Functional Ecology 25, 358367.Google Scholar
Casteel, C., Walling, L.L. & Paine, T. (2006) Behavior and biology of the tomato psyllid, Bactericerca cockerelli, in response to the Mi-1.2 gene. Entomologia Experimentalis et Applicata 121, 6772.Google Scholar
Century, K.S., Lagman, R.A., Adkisson, M., Morlan, J., Tobias, R., Schwartz, K., Smith, A., Love, J., Ronald, P.C. & Whalen, M.C. (1999) Developmental control of Xa21-mediated disease resistance in rice. Plant Journal 20, 231236.Google Scholar
De Barro, P.J., Liu, S.S., Boykin, L.M. & Dinsdale, A.B. (2011) Bemisia tabaci: a statement of species status. Annual Review of Entomology 56, 119.Google Scholar
Dixon, M.S., Golstein, C., Thomas, C.M., van Der Biezen, E.A. & Jones, J.D. (2000) Genetic complexity of pathogen perception by plants: the example of Rcr3, a tomato gene required specifically by Cf-2. Proceedings of the National Academy of Sciences of the United States of America 97, 88078814.Google Scholar
Dropkin, V.H. (1969) The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature. Phytopathology 59, 16321637.Google Scholar
Ebrahim, S., Usha, K. & Singh, B. (2011) Pathogenesis related (PR) proteins in plant defense mechanism. pp. 10431054 in Mendez-Vilas, A. (Ed.) Science against Microbial Pathogens: Communicating Current Research and Technological Advances. 3rd edn. Vol. 2. Badajoz, Spain, Formatex Research Centre Publisher.Google Scholar
Ellsworth, P.C. & Martinez-Carrillo, J.L. (2001) IPM for Bemisia tabaci: a case study from North America. Crop Protection 20, 853869.Google Scholar
Goel, R.K. & Gupta, A.K. (1990) Host age in relation to resistance in rice to bacterial blight caused by Xanthomonas campestris pv. oryzae. Tropical Agriculture 67, 368370.Google Scholar
Goggin, F.L., Shah, G., Williamson, V.M. & Ullman, D.E. (2004) Developmental regulation of Mi-mediated aphid resistance is independent of Mi-1.2 transcript levels. Molecular Plant-Microbe Interactions 17, 532536.Google Scholar
González-Zamora, J.E. & Gallardo, J.M. (1999) Desarrollo y capacidad reproductiva de Bemisia tabaci (Gennadius) (Homoptera; Aleyrodidae) en pimiento a tres temperaturas. Boletín de Sanidad Vegetal-Plagas 25, 311.Google Scholar
Ho, J.-Y., Weide, R., Ma, H.M., van Wordragen, M.F., Lambert, K.N., Koornneef, M., Zabel, P. & Williamson, V.M. (1992) The root-knot nematode resistance gene Mi in tomato: construction of a molecular linkage map and identification of dominant cDNA markers in resistant genotypes. Plant Journal 2, 971982.Google Scholar
Islam, M.T. & Slunziang, R. (2007) Development and reproduction of Bemisia tabaci on three tomato varieties. Journal of Entomology 4, 231236.Google Scholar
Kaloshian, I., Lange, W.H. & Williamson, V.M. (1995) An aphid-resistance locus is tightly linked to the nematode-resistance gene, Mi, in tomato. Proceedings of the National Academy of Sciences 92, 622625.Google Scholar
Kaloshian, I., Kinsey, M.G., Ullman, D.E. & Williamson, V.M. (1997) The impact of Meu1-mediated resistance in tomato on longevity, fecundity and behavior of the potato aphid, Macrosiphum euphorbiae. Entomologia Experimentalis et Applicata 83, 181187.Google Scholar
Laterrot, H. (1987) Near-isogenic tomato lines in Moneymaker type with different genes for disease resistances. Tomato Genetics Cooperative Report 37, 91.Google Scholar
Leite, G.L.D., Picanço, M., Guedes, R.N.C. & Zanuncio, J.C. (2001) Role of plant age in the resistance of Lycopersicon hirsutum f. glabratum to the tomato leafminer Tuta absoluta (Lepidoptera : Gelechiidae). Scientia Horticulturae 89, 103113.Google Scholar
Mansaray, A. & Sundufu, A.J. (2009) Oviposition, development and survivorship of the sweetpotato whitefly Bemisia tabaci on soybean, Glycine max, and the garden bean, Phaseolus vulgaris. Journal of Insect Science 9, 16.Google Scholar
Martínez de Ilarduya, O. & Kaloshian, I. (2001) Mi-1.2 Transcripts accumulate ubiquitously in resistant Lycopersicon esculentum. Journal of Nematology 33, 116120.Google Scholar
Martínez de Ilarduya, O., Moore, A.E. & Kaloshian, I. (2001) The tomato Rme1 locus is required for Mi-1-mediated resistance to root-knot nematodes and the potato aphid. Plant Journal 27, 417425.Google Scholar
Martínez De Ilarduya, O., Nombela, G., Hwang, C.-F., Williamson, V.M., Muñiz, M. & Kaloshian, I. (2004) Rme1 is necessary for Mi-1-mediated resistance and acts early in the resistance pathway. Molecular Plant-Microbe Interactions 17, 5561.Google Scholar
Mew, T.W. (1987) Current status and future prospects of research on bacterial blight of rice. Annual Review of Phytopathology 25, 359382.Google Scholar
Musa, P.D. & Ren, S.-X. (2005) Development and reproduction of Bemisia tabaci (Homoptera: Aleyrodidae) on three bean species. Insect Science 12, 2530.Google Scholar
Nombela, G., Beitia, F.J. & Muñiz, M. (2000) Variation in tomato host response to Bemisia tabaci (Hemiptera: Aleyrodidae) in relation to acyl sugar content and presence of the nematode and potato aphid resistance gene Mi. Bulletin of Entomological Research 90, 161167.Google Scholar
Nombela, G., Beitia, F.J. & Muñiz, M. (2001) A differential interaction study of Bemisia tabaci Q-biotype on commercial tomato varieties with or without the Mi resistance gene, and comparative host responses with the B-biotype. Entomologia Experimentalis et Applicata 98, 339344.Google Scholar
Nombela, G., Williamson, V.M. & Muñiz, M. (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Molecular Plant-Microbe Interactions 16, 645649.Google Scholar
Ogawa, T. (1993) Methods and strategy for monitoring race distribution and identification of resistance genes to bacterial leaf blight (Xanthomonas campestris pv. oryzae) in rice. Japan Agricultural Research Quarterly 27, 7180.Google Scholar
Panter, S.N. & Jones, D.A. (2002) Age-related resistance to plant pathogens. Advances in Botanical Research 38, 251280.Google Scholar
Panter, S.N., Hammond-Kosack, K.E., Harrison, K., Jones, J.D.G. & Jones, D.A. (2002) Developmental control of promoter activity is not responsible for mature onset of Cf-9B-mediated resistance to leaf mold in tomato. Molecular Plant-Microbe Interactions 15, 10991107.Google Scholar
Pascual, S., Avilés, M., Nombela, G., Muñiz, M. & Beitia, F. (2000) Development of Bemisia tabaci (biotype Q) on tomato cultivars with/without the Mi gene. Med. Fac. Landbouww. Univ. Gent. 65, 291292.Google Scholar
Qi, Z. & Mew, T.W. (1985) Adult-plant resistance of rice cultivars to bacterial blight. Plant Disease 69, 896898.Google Scholar
Qiu, B.-L., Ren, S.-X., Mandour, N.S. & Lin, L. (2003) Effect of temperature on the development and reproduction of Bemisia tabaci B biotype (Homoptera: Aleyrodidae). Insect Science 10, 4349.Google Scholar
Roberts, P.A. & Thomason, I.J. (1986) Variability in reproduction of isolates of Meloidogyne incognita and M. javanica on resistant tomato genotypes. Plant Disease 70, 547551.Google Scholar
Rossi, M., Goggin, F.L., Milligan, S.B., Kaloshian, I., Ullman, D.E. & Williamson, V.M. (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of the National Academy of Sciences 95, 97509754.Google Scholar
Statgraphics (1997) Statgraphics Plus for Windows 3.1. Englewood Cliffs, NJ, USA, Statistical Graphics Corp.Google Scholar
STATSOFT (1994) Statistica Version 4.5 for the Windows Operating System. Reference for Statistical Procedures. Tulsa, OK, USA, StatSoft.Google Scholar
Van Ooijen, G., Mayr, G., Kasiem, M.M.A., Albrecht, M., Cornelissen, B.J.C. & Takken, F.L.W. (2008) Structure-function analysis of the NB-ARC domain of plant disease resistance proteins. Journal of Experimental Botany 59, 13831397.Google Scholar
Visker, M.H.P.W., Keizer, L.C.P., Budding, D.J., Van Loon, L.C., Colon, L.T. & Struik, P.C. (2003) Leaf position prevails over plant age and leaf age in reflecting resistance to late blight in potato. Phytopathology 93, 666674.Google Scholar
Yang, T.-C. & Chi, H. (2006) Life tables and development of Bemisia argentifolii (Homoptera: Aleyrodidae) at different temperatures. Journal of Economic Entomology 99, 691698.Google Scholar
Zhang, G.-F. & Wan, F.-H. (2012) Suitability changes with host leaf age for Bemisia tabaci B Biotype and Trialeurodes vaporariorum. Environmental Entomology 41, 11251130.Google Scholar