The Sw-5 gene cluster : Tomato breeding and research toward orthotospovirus disease control
Oliveira, Athos S. de; Boiteux, Leonardo S. ; Kormelink, Richard ; Resende, Renato O. - \ 2018
Frontiers in Plant Science 9 (2018). - ISSN 1664-462X
NB-LRR - NLR - Orthotospovirus - Resistance - Sw-5 - Sw-5b - Tomato
The Sw-5 gene cluster encodes protein receptors that are potentially able to recognize microbial products and activate signaling pathways that lead to plant cell immunity. Although there are several Sw-5 homologs in the tomato genome, only one of them, named Sw-5b, has been extensively studied due to its functionality against a wide range of (thrips-transmitted) orthotospoviruses. The Sw-5b gene is a dominant resistance gene originally from a wild Peruvian tomato that has been used in tomato breeding programs aiming to develop cultivars with resistance to these viruses. Here, we provide an overview starting from the first reports of Sw-5 resistance, positional cloning and the sequencing of the Sw-5 gene cluster from resistant tomatoes and the validation of Sw-5b as the functional protein that triggers resistance against orthotospoviruses. Moreover, molecular details of this plant–virus interaction are also described, especially concerning the roles of Sw-5b domains in the sensing of orthotospoviruses and in the signaling cascade leading to resistance and hypersensitive response.
Cell death triggering and effector recognition by Sw-5 SD-CNL proteins from resistant and susceptible tomato isolines to Tomato spotted wilt virus
Silva de Oliveira, A. ; Koolhaas, Ivo ; Boiteux, L.S. ; Caldararu, O. ; Petrescu, A.J. ; Resende, R. ; Kormelink, R.J.M. - \ 2016
Molecular Plant Pathology 17 (2016)9. - ISSN 1464-6722 - p. 1442 - 1454.
Only a limited number of dominant resistance genes acting against plant viruses have been cloned, and further functional studies of these have been almost entirely limited to the resistance genes Rx against Potato virus X (PVX) and N against Tobacco mosaic virus (TMV). Recently, the cell-to-cell movement protein (NSM) of Tomato spotted wilt virus (TSWV) has been identified as the avirulence determinant (Avr) of Sw-5b-mediated resistance, a dominant resistance gene which belongs to the class of SD-CC-NB-LRR (Solanaceae domain-coiled coil-nucleotide-binding-leucine-rich repeat, SD-CNL) resistance genes. On transient expression of the NSM protein in tomato and transgenic Nicotiana benthamiana harbouring the Sw-5b gene, a hypersensitive cell death response (HR) is triggered. Here, it is shown that high accumulation of the Sw-5b protein in N. benthamiana leaves, achieved by co-expression of the Sw-5b protein with RNA silencing suppressors (RSSs), leads to auto-activity in the absence of NSM. In a similar approach, Sw-5a, the highest conserved paralogue of Sw-5b from Solanum peruvianum, also triggered HR by auto-activation, whereas the highest conserved orthologue from susceptible S. lycopersicum, named Sw-5aS, did not. However, neither of the last two homologues was able to trigger an NSM-dependent HR. Truncated and mutated versions of these Sw-5 proteins revealed that the NB-ARC [nucleotide-binding adaptor shared by Apaf-1 (from humans), R proteins and CED-4 (from nematodes)] domain is sufficient for the triggering of HR and seems to be suppressed by the SD-CC domain. Furthermore, a single mutation was sufficient to restore auto-activity within the NB-ARC domain of Sw-5aS. When the latter domain was fused to the Sw-5b LRR domain, NSM-dependent HR triggering was regained, but not in the presence of its own Sw-5aS LRR domain. Expression analysis in planta revealed a nucleocytoplasmic localization pattern of Sw-5b, in which the SD-CC domain seems to be required for nuclear translocation. Although the Sw-5 N-terminal CC domain, in contrast with Rx, contains an additional SD, most findings from this study support a conserved role of domains within NB-LRR (NLR) proteins against plant viruses.
Resistance to Tospoviruses in Vegetable Crops : Epidemiological and Molecular Aspects
Turina, Massimo ; Kormelink, Richard ; Resende, Renato O. - \ 2016
Annual Review of Phytopathology 54 (2016). - ISSN 0066-4286 - p. 347 - 371.
Avirulence determinant - Pepper - R gene - Taxonomy - Tomato - TSWV
During the past three decades, the economic impact of tospoviruses has increased, causing high yield losses in a variety of crops and ornamentals. Owing to the difficulty in combating thrips vectors with insecticides, the best way to limit/prevent tospovirus-induced diseases involves a management strategy that includes virus resistance. This review briefly presents current tospovirus taxonomy, diversity, molecular biology, and cytopathology as an introduction to a more extensive description of the two main resistance genes employed against tospoviruses: the Sw5 gene in tomato and the Tsw in pepper. Natural and experimental resistance-breaking (RB) isolates allowed the identification of the viral avirulence protein triggering each of the two resistance gene products; epidemiology of RB isolates is discussed to reinforce the need for allelic variants and the need to search for new/alternative resistance genes. Ongoing efforts for alternative resistance strategies are described not only for Tomato spotted wilt virus (TSWV) in pepper and tomato but also for other vegetable crops heavily impacted by tospoviruses.
Climate seasonality limits leaf carbon assimilation and wood productivity in tropical forests
Wagner, Fabien H. ; Hérault, Bruno ; Bonal, Damien ; Stahl, Clément ; Anderson, Liana O. ; Baker, Timothy R. ; Becker, Gabriel Sebastian ; Beeckman, Hans ; Boanerges Souza, Danilo ; Botosso, Paulo Cesar ; Bowman, David M.J.S. ; Bräuning, Achim ; Brede, Benjamin ; Brown, Foster Irving ; Camarero, Jesus Julio ; Camargo, Plínio Barbosa ; Cardoso, Fernanda C.G. ; Carvalho, Fabrício Alvim ; Castro, Wendeson ; Chagas, Rubens Koloski ; Chave, Jérome ; Chidumayo, Emmanuel N. ; Clark, Deborah A. ; Costa, Flavia Regina Capellotto ; Couralet, Camille ; Silva Mauricio, Paulo Henrique Da; Dalitz, Helmut ; Castro, Vinicius Resende De; Freitas Milani, Jaçanan Eloisa De; Oliveira, Edilson Consuelo De; Souza Arruda, Luciano De; Devineau, Jean-Louis ; Drew, David M. ; Dünisch, Oliver ; Durigan, Giselda ; Elifuraha, Elisha ; Fedele, Marcio ; Ferreira Fedele, Ligia ; Figueiredo Filho, Afonso ; Finger, César Augusto Guimarães ; Franco, Augusto César ; Freitas Júnior, João Lima ; Galvão, Franklin ; Gebrekirstos, Aster ; Gliniars, Robert ; Lima De Alencastro Graça, Paulo Maurício ; Griffiths, Anthony D. ; Grogan, James ; Guan, Kaiyu ; Homeier, Jürgen ; Kanieski, Maria Raquel ; Kho, Lip Khoon ; Koenig, Jennifer ; Kohler, Sintia Valerio ; Krepkowski, Julia ; Lemos-filho, José Pires ; Lieberman, Diana ; Lieberman, Milton Eugene ; Lisi, Claudio Sergio ; Longhi Santos, Tomaz ; López Ayala, José Luis ; Maeda, Eduardo Eijji ; Malhi, Yadvinder ; Maria, Vivian R.B. ; Marques, Marcia C.M. ; Marques, Renato ; Maza Chamba, Hector ; Mbwambo, Lawrence ; Melgaço, Karina Liana Lisboa ; Mendivelso, Hooz Angela ; Murphy, Brett P. ; O'Brien, Joseph J. ; Oberbauer, Steven F. ; Okada, Naoki ; Pélissier, Raphaël ; Prior, Lynda D. ; Roig, Fidel Alejandro ; Ross, Michael ; Rossatto, Davi Rodrigo ; Rossi, Vivien ; Rowland, Lucy ; Rutishauser, Ervan ; Santana, Hellen ; Schulze, Mark ; Selhorst, Diogo ; Silva, Williamar Rodrigues ; Silveira, Marcos ; Spannl, Susanne ; Swaine, Michael D. ; Toledo, José Julio ; Toledo, Marcos Miranda ; Toledo, Marisol ; Toma, Takeshi ; Tomazello Filho, Mario ; Valdez Hernández, Juan Ignacio ; Verbesselt, Jan ; Vieira, Simone Aparecida ; Vincent, Grégoire ; Volkmer De Castilho, Carolina ; Volland, Franziska ; Worbes, Martin ; Zanon, Magda Lea Bolzan ; Aragão, Luiz E.O.C. - \ 2016
Biogeosciences 13 (2016)8. - ISSN 1726-4170 - p. 2537 - 2562.
The seasonal climate drivers of the carbon cycle in tropical forests remain poorly known, although these forests account for more carbon assimilation and storage than any other terrestrial ecosystem. Based on a unique combination of seasonal pan-tropical data sets from 89 experimental sites (68 include aboveground wood productivity measurements and 35 litter productivity measurements), their associated canopy photosynthetic capacity (enhanced vegetation index, EVI) and climate, we ask how carbon assimilation and aboveground allocation are related to climate seasonality in tropical forests and how they interact in the seasonal carbon cycle. We found that canopy photosynthetic capacity seasonality responds positively to precipitation when rainfall is < 2000 mm yr−1 (water-limited forests) and to radiation otherwise (light-limited forests). On the other hand, independent of climate limitations, wood productivity and litterfall are driven by seasonal variation in precipitation and evapotranspiration, respectively. Consequently, light-limited forests present an asynchronism between canopy photosynthetic capacity and wood productivity. First-order control by precipitation likely indicates a decrease in tropical forest productivity in a drier climate in water-limited forest, and in current light-limited forest with future rainfall < 2000 mm yr−1.
The Tomato spotted wilt virus cell-to-cell movement protein (NSM) triggers a hypersensitive response in Sw-5 containing resistant tomato lines and Nicotiana benthamiana transformed with the functional Sw-5b resistance gene copy.
Hallwass, M. ; Silva de Oliveira, A. ; Dianese, E.C. ; Lohuis, D. ; Boiteux, L.S. ; Inoue-Nagata, A.K. ; Resende, R.O. de; Kormelink, R.J.M. - \ 2014
Molecular Plant Pathology 15 (2014)9. - ISSN 1464-6722 - p. 871 - 880.
mosaic-virus - lycopersicon-esculentum - nonstructural protein - capsicum-chinense - coat protein - plant-cells - rna segment - tswv - tospovirus - tobacco
Although the Sw-5 gene cluster has been cloned, and Sw-5b has been identified as the functional gene copy that confers resistance to Tomato spotted wilt virus (TSWV), its avirulence (Avr) determinant has not been identified to date. Nicotiana tabacum SR1 plants transformed with a copy of the Sw-5b gene are immune without producing a clear visual response on challenge with TSWV, whereas it is shown here that N.benthamiana transformed with Sw-5b gives a rapid and conspicuous hypersensitive response (HR). Using these plants, from all structural and non-structural TSWV proteins tested, the TSWV cell-to-cell movement protein (NSM) was confirmed as the Avr determinant using a Potato virus X (PVX) replicon or a non-replicative pEAQ-HT expression vector system. HR was induced in Sw-5b-transgenic N.benthamiana as well as in resistant near-isogenic tomato lines after agroinfiltration with a functional cell-to-cell movement protein (NSM) from a resistance-inducing (RI) TSWV strain (BR-01), but not with NSM from a Sw-5 resistance-breaking (RB) strain (GRAU). This is the first biological demonstration that Sw-5-mediated resistance is triggered by the TSWV NSM cell-to-cell movement protein.
Development of a locus-specific, co-dominant SCAR marker for assisted-selection of the Sw-5 (Tospovirus resistance) gene cluster in a wide range of tomato accessions
Dianese, E.C. ; Fonseca, M.E.N. ; Goldbach, R.W. ; Kormelink, R.J.M. ; Inoue-Nagata, A.K. ; Resende, R.O. de; Boiteux, L.S. - \ 2010
Molecular Breeding 25 (2010)1. - ISSN 1380-3743 - p. 133 - 142.
spotted-wilt-virus - lycopersicon-esculentum - thrips transmission - tswv resistance - rapd markers - peruvianum - sw5
The best levels of broad-spectrum Tospovirus resistance reported in tomatoes thus far are conferred by the Sw-5 locus. This locus contains at least five paralogues (denoted Sw-5a through Sw-5e), of which Sw-5b represents the actual resistance gene. Here we evaluated a panel of seven PCR primer pairs matching different sequences within a genomic region spanning the Sw-5a and Sw-5b gene cluster. Primer efficiency evaluation was done employing tomato isolines with and without the Sw-5 locus. One primer pair produced a single and co-dominant polymorphism between susceptible and resistant isolines. Sequence analysis of these amplicons indicated that they were specific for the Sw-5 locus and their differences were due to insertions/deletions. The polymorphic SCAR amplicon encompass a conserved sequence of the promoter region of the functional Sw-5b gene, being located in the position -31 from its open reading frame. This primer pair was also evaluated in field assays and with a collection of accessions known to be either susceptible or resistant to tospoviruses. An almost complete correlation was found between resistance under greenhouse/field conditions and the presence of the marker. Therefore, this primer pair is a very useful tool in marker-assisted selection systems in a large range of tomato accessions.
Papaya Lethal Yellowing Virus (PLYV) Infects Vasconcellea cauliflora
Amaral, P.P.R. ; Resende, R.O. de; Souza, M.T. - \ 2006
Fitopatologia Brasileira 31 (2006)5. - ISSN 0100-4158 - p. 517 - 517.
Papaya lethal yellowing virus (PLYV) é um dos três vírus descritos infectando mamoeiros (Carica papaya L.) no Brasil. Vasconcellea cauliflora (Jacq.) A. DC., antes denominada de Carica cauliflora (Jacq.), é uma reconhecida fonte de resistência natural ao Papaya ringspot virus (PRSV), causador da "Mancha Anelar" ou "Mosaico" do mamoeiro. Neste estudo é demonstrado que V. cauliflora pode ser infectada por PLYV mediante inoculação mecânica. Esta é a segunda hospedeira de PLYV descrita até o momento. Por ser infectado por PLYV, mas não PRSV, esta espécie da família das Caricaceas pode ser utilizada para separação destes vírus quando em infecção mista numa planta de C. papaya
|Synergism between crini- and tospoviruses results in suppression of host defenses in tomato
Canizares, C. ; Garcia-Cano, E. ; Resende, R.O. de; Prins, M.W. ; Moriones, E. - \ 2006
In: EMBO Workshop in Plant Virology 2006, Suppression and Circumvention of Host Defence by Plant Viruses, Helsinki, Finland, 1-5 July 2006. - Helsinki : - p. 62 - 62.
Pepper yellow mosaic virus, a new potyvirus in sweet-pepper. Archives of Virology
Inoue-Nagata, A.K. ; Fonseca, M.E.N. ; Resende, R.O. de; Boiteux, L.S. ; Monte, D.C. ; Dusi, A.N. ; Ávila, A.C. de; Vlugt, R.A.A. van der - \ 2002
Archives of Virology 147 (2002)4. - ISSN 0304-8608 - p. 849 - 855.
A potyvirus was found causing yellow mosaic and veinal banding in sweetpepper in Central and Southeast Brazil. The sequence analysis of the 3' terminal region of the viral RNA revealed a coat protein of 278 amino acids, followed by 275 nucleotides in the 3'-untranslated region preceding a polyadenylated tail. The virus shared 77.4% coat protein amino acid identity with Pepper severe mosaic virus, the closest Potyvirus species. The 3'-untranslated region was highly divergent from other potyviruses. Based on these results, the virus found in sweetpepper plants could be considered as a new potyvirus. The name Pepper yellow mosaic virus (PepYMV) is suggested
Characterization of a tospovirus isolate of iris yellow spot virus associated with a disease in onion fields in Brazil
Pozzer, L. ; Bezerra, I.C. ; Kormelink, R. ; Prins, M. ; Peters, D. ; Resende, O. de; Avila, A.C. de - \ 1999
Plant Disease 83 (1999)4. - ISSN 0191-2917 - p. 345 - 350.
Increase of tospoviral diversity in Brazil with the identification of two new tospovirus species, one from Chrysanthemum and one from Zucchini
Bezerra, I.C. ; Resende, R.O. de; Pozzer, L. ; Nagata, T. ; Kormelink, R. ; Avila, A.C. de - \ 1999
Phytopathology 89 (1999)9. - ISSN 0031-949X - p. 823 - 830.
|Tomato spotted wilt virus: genome organization, transmission, and symptom induction.
Goldbach, R. ; Kormelink, R. ; O. Resende, R. de; Avila, A.C. de; Poelwijk, F. van; Lent, J. van; Wijkamp, I. ; Prins, M. ; Peters, D. - \ 1995
In: Biotechnology and plant protection / Bills, D.D., Kung, Shain-dow, - p. 297 - 311.
|Effects of the host and the inocula concentration in the generation of defective interfering RNAs of tospoviruses.
Resende, R.O. ; Avila, A.C. de; Goldbach, R. ; Peters, D. - \ 1994
In: Fitopatologia Brasileira 19 (1994)
Distinct levels of relationships between tospovirus isolates.
Avila, A.C. de; Haan, P. de; Smeets, M.L.L. ; O. Resende, R. de; Kormelink, R. ; Kitajima, E.W. ; Goldbach, R.W. ; Peters, D. - \ 1993
Archives of Virology 128 (1993). - ISSN 0304-8608 - p. 211 - 227.
Classification of tospoviruses based on phylogeny of nucleoprotein gene sequences.
Avila, A.C. de; Haan, P. de; Kormelink, R. ; O. Resende, R. de; Goldbach, R.W. ; Peters, D. - \ 1993
Journal of General Virology 74 (1993). - ISSN 0022-1317 - p. 153 - 159.
|Characterization of defective interfering L RNAs of tomato spotted wilt virus, a bunyavirus infecting plants.
O. Resende, R. de; Haan, P. de; Poelwijk, F. van; Avila, A.C. de; Kormelink, R. ; Goldbach, R.W. ; Peters, D. - \ 1992
In: Ned. Kring Plantevirologie (1992)
|Tomato spotted wilt virus: genome organization, transmission and symptom expression.
Goldbach, R.W. ; Kormelink, R. ; Haan, P. de; O. Resende, R. de; Avila, A.C. de; Poelwijk, F. van; Lent, J.W.M. van; Wijkamp, I. ; Prins, M. ; Peters, D. - \ 1992
In: Abstract 5th Int. Symp. Biotechnology and plant protection, Univ. Maryland, USA - p. 5 - 5.
|Characterization of DI L-RNAmolecules of tomato spotted wilt virus.
O. Resende, R. de; Haan, P. de; Kormelink, R. ; Avila, A.C. de; Goldbach, R.W. ; Peters, D. - \ 1992
In: SON Werkgemeenschap Nucleinezuren. Lunteren (1992)
|Characterization of DI L-RNAs of tomato spotted wilt virus.
O. Resende, R. de; Haan, P. de; Poelwijk, F. van; Avila, A.C. de; Goldbach, R.W. ; Peters, D. - \ 1992
In: Abstract 11th Ann. Meeting Am. Soc. Virology, Ithaca (1992)
|Comparative cytological and immunogold labelling studies on different isolates of tomato spotted wilt virus.
Kitajima, E.W. ; Avila, A.C. de; O. Resende, R. de; Goldbach, R.W. ; Peters, D. - \ 1992
Journal of submicroscopic cytology and pathology 24 (1992). - ISSN 1122-9497 - p. 1 - 14.