Wheat TaLr35PR2 gene is required for Lr35-mediated adult plant resistance against leaf rust fungus
Fang Liang
A , Xiong Du B , Jiarui Zhang A , Xiaoying Li A , Fei Wang A , Haiyan Wang A C and Daqun Liu A
+ Author Affiliations
- Author Affiliations
A Centre of Plant Disease and Plant Pests of Hebei Province, College of Plant Protection, Hebei Agricultural University, Baoding 071001, China.
B College of Agronomy, Hebei Agricultural University, Baoding 071001, China.
C Corresponding author. Email: ndwanghaiyan@163.com.
Functional Plant Biology 47(1) 26-37 https://doi.org/10.1071/FP18340
Submitted: 26 October 2018 Accepted: 26 July 2019 Published: 9 December 2019
Abstract
In this study we analysed the expression patterns of TaLr35PR2 and confirmed its role in Lr35-mediated adult resistance to leaf rust fungus. β-1,3-glucanase, a pathogenesis-related protein, has a critical function in plant defence response against fungal pathogens. We previously described the full-length gene TaLr35PR2, which encodes a protein exhibiting amino acid and structural similarity to β-1,3-glucanase, in the wheat near-isogenic line TcLr35 (GenBank accession number DQ294235.1). This work aimed to further assess TaLr35PR2 expression patterns and function in Lr35-mediated adult resistance to Puccinia triticina. Immunoblot was performed to demonstrate that TaLr35PR2 expression was triggered early by P. triticina, with expression levels markedly elevated in incompatible interaction compared with those in compatible one. Additionally, TaLr35PR2 accumulation steadily increased and overtly peaked after challenge with P. triticina through the various developmental stages of TcLr35 wheat, and remaining at similar levels after mock inoculation. Furthermore, TaLr35PR2 expression was significantly reduced in barley stripe mosaic virus (BSMV)-induced gene knockdown plants, in which pathological assessment revealed that TaLr35PR2-silenced plants was obviously susceptible to leaf rust fungus compared with wild-type TcLr35, indicating that Lr35-mediated resistance to leaf rust was diminished. These findings strongly suggest that TaLr35PR2 is involved in Lr35-mediated wheat defence against the leaf rust pathogen.
Additional keywords: adult plant resistance, expression profiles, pathogenesis-related protein 2, Puccinia triticina, wheat.
References
Anguelova VS, Westhuizen AJVD, Pretorius ZA (1999) Intercellular proteins and β-1,3-glucanase activity associated with leaf rust resistance in wheat. Physiologia Plantarum 106, 393–401.| Intercellular proteins and β-1,3-glucanase activity associated with leaf rust resistance in wheat.Crossref | GoogleScholarGoogle Scholar |
Bol JF, Linthorst HJM, Cornelissen BJC (1990) Plant pathogenesis-related proteins induced by virus infection. Annual Review of Phytopathology 28, 113–138.
| Plant pathogenesis-related proteins induced by virus infection.Crossref | GoogleScholarGoogle Scholar |
Bronner R, Westphal E, Dreger F (1991) Pathogenesis-related proteins in Solanum dulcamara L. resistant to the gall mite Aceria cladophthirus (Nalepa) (syn Eriophyes cladophthirus Nal.). Physiological and Molecular Plant Pathology 38, 93–104.
| Pathogenesis-related proteins in Solanum dulcamara L. resistant to the gall mite Aceria cladophthirus (Nalepa) (syn Eriophyes cladophthirus Nal.).Crossref | GoogleScholarGoogle Scholar |
Burch-Smith TM, Anderson J, Martin GKS (2004) Applications and advantages of virus-induced gene silencing for gene function studies in plants. The Plant Journal 39, 734–746.
| Applications and advantages of virus-induced gene silencing for gene function studies in plants.Crossref | GoogleScholarGoogle Scholar | 15315635PubMed |
Chen XM (2014) Integration of cultivar resistance and fungicide application for control of wheat stripe rust. Canadian Journal of Plant Pathology 36, 311–326.
| Integration of cultivar resistance and fungicide application for control of wheat stripe rust.Crossref | GoogleScholarGoogle Scholar |
Gao L, Wang S, Li XY, Wei XJ, Zhang YJ, Wang HY, Liu DQ (2015) Expression and functional analysis of a pathogenesis-related protein 1 gene, TcLr19PR1, involved in wheat resistance against leaf rust fungus. Plant Molecular Biology Reporter 33, 797–805.
| Expression and functional analysis of a pathogenesis-related protein 1 gene, TcLr19PR1, involved in wheat resistance against leaf rust fungus.Crossref | GoogleScholarGoogle Scholar |
Germán S, Barcellos A, Chaves M, Kohli M, Campos P, Viedma LD (2007) The situation of common wheat rusts in the southern cone of America and perspectives for control. Australian Journal of Agricultural Research 58, 620–630.
| The situation of common wheat rusts in the southern cone of America and perspectives for control.Crossref | GoogleScholarGoogle Scholar |
Holzberg S, Brosio P, Gross C, Pogue GP (2002) Barley stripe mosaic virus-induced gene silencing in a monocot plant. The Plant Journal 30, 315–327.
| Barley stripe mosaic virus-induced gene silencing in a monocot plant.Crossref | GoogleScholarGoogle Scholar | 12000679PubMed |
Hong TY, Meng M (2003) Biochemical characterization and antifungal activity of an endo-1,3-β-glucanase of Paenibacillus sp. isolated from garden soil. Applied Microbiology and Biotechnology 61, 472–478.
| Biochemical characterization and antifungal activity of an endo-1,3-β-glucanase of Paenibacillus sp. isolated from garden soil.Crossref | GoogleScholarGoogle Scholar | 12764561PubMed |
Jacobs KA, Collins-Racie LA, Colbert M, Duckett MK, Golden-Fleet M, Kelleher K (1997) A genetic selection for isolating cDNAs encoding secreted proteins. Gene 198, 289–296.
| A genetic selection for isolating cDNAs encoding secreted proteins.Crossref | GoogleScholarGoogle Scholar | 9370294PubMed |
Keen NT, Yoshikawa M (1983) β-1,3-Endoglucanase from soybean releases elicitor-active carbohydrates from fungus cell walls. Plant Physiology 71, 460
| β-1,3-Endoglucanase from soybean releases elicitor-active carbohydrates from fungus cell walls.Crossref | GoogleScholarGoogle Scholar | 16662849PubMed |
Kerber ER, Dyck PL (1990) Transfer to hexaploid wheat of linked genes for adult-plant leaf rust. Genome 33, 530–537.
| Transfer to hexaploid wheat of linked genes for adult-plant leaf rust.Crossref | GoogleScholarGoogle Scholar |
Kessmann H, Staub T, Ligon J, Oostendorp M, Ryals J (1994) Activation of systemic acquired disease resistance in plants. European Journal of Plant Pathology 100, 359–369.
| Activation of systemic acquired disease resistance in plants.Crossref | GoogleScholarGoogle Scholar |
Lacomme C, Hrubikova K, Hein I (2003) Enhancement of virus-induced gene silencing through viral-based production of inverted-repeats. Plant J 34, 543–553.
| Enhancement of virus-induced gene silencing through viral-based production of inverted-repeats.Crossref | GoogleScholarGoogle Scholar | 12753592PubMed | [In Chinese]
Li X, Gao L, Zhang Y, Wang H, Liu D (2014) Expression and analysis of β-1,3-glucanase gene in wheat TcLr35 induced by wheat leaf rust pathogen and signal molecule. Scientia Agricultura Sinica 47, 2774–2783.
Li X, Gao L, Zhang W, Liu J, Zhang Y, Wang H, Liu D (2015) Characteristic expression of wheat gene in response to infection by the leaf rust pathogen. Journal of Plant Interactions 10, 132–141.
| Characteristic expression of wheat gene in response to infection by the leaf rust pathogen.Crossref | GoogleScholarGoogle Scholar |
Lind V, Gultyaeva E (2007) Virulence frequencies of Puccinia triticina in Germany and the European regions of the Russian federation. Journal of Phytopathology 155, 13–21.
| Virulence frequencies of Puccinia triticina in Germany and the European regions of the Russian federation.Crossref | GoogleScholarGoogle Scholar |
Liu B, Xue X, Cui S, Zhang X, Han Q, Zhu L, Liang X, Wang X, Huang L, Chen X, Kang Z (2010) Cloning and characterization of a wheat β-1,3-glucanase gene induced by the stripe rust pathogen Puccinia striiformis f. sp. tritici. Molecular Biology Reports 37, 1045–1052.
| Cloning and characterization of a wheat β-1,3-glucanase gene induced by the stripe rust pathogen Puccinia striiformis f. sp. tritici.Crossref | GoogleScholarGoogle Scholar | 19757158PubMed |
Liu D, He X, Li W, Chen C, Ge F (2013) A β-1,3-glucanase gene expressed in fruit of Pyrus pyrifolia enhances resistance to several pathogenic fungi in transgenic tobacco. European Journal of Plant Pathology 135, 265–277.
| A β-1,3-glucanase gene expressed in fruit of Pyrus pyrifolia enhances resistance to several pathogenic fungi in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |
Lo Presti L, Lanver D, Schweizer G, Tanaka S, Liang L, Tollot M, Zuccaro A, Reissmann S, Kahmann R (2015) Fungal effectors and plant susceptibility. Annual Review of Plant Biology 66, 513–545.
| Fungal effectors and plant susceptibility.Crossref | GoogleScholarGoogle Scholar | 25923844PubMed |
Lu R, Martin-Hernandez AM, Peart JR, Malcuit I, Baulcombe DC (2003) Virus-induced gene silencing in plants. Methods 30, 296–303.
Mauch F, Staehelin LA (1989) Functional implications of the subcellular localization of ethylene-induced chitinase and beta-1,3-glucanase in bean leaves. The Plant Cell 1, 447–457.
| Functional implications of the subcellular localization of ethylene-induced chitinase and beta-1,3-glucanase in bean leaves.Crossref | GoogleScholarGoogle Scholar | 12359894PubMed |
McCallum B, Fetch T, Chong J (2007) Cereal rust control in Canada. Australian Journal of Agricultural Research 58, 639–647.
Muthukrishnan S, Liang GH, Trick HN, Gill BS (2001) Pathogenesis related proteins and their genes in cereals. Plant Cell, Tissue and Organ Culture 64, 93–114.
| Pathogenesis related proteins and their genes in cereals.Crossref | GoogleScholarGoogle Scholar |
O’Kennedy MM, Crampton BG, Lorito M, Chakauya E, Breese WA, Burger JT (2011) Expression of a β-1,3-glucanase from a biocontrol fungus in transgenic pearl millet. South African Journal of Botany 77, 335–345.
| Expression of a β-1,3-glucanase from a biocontrol fungus in transgenic pearl millet.Crossref | GoogleScholarGoogle Scholar |
Oh SK, Young C, Lee M, Oliva R, Bozkurt TO, Cano LM (2009) In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the Solanum bulbocastanum disease resistance protein Rpi-blb2. The Plant Cell 21, 2928
| In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the Solanum bulbocastanum disease resistance protein Rpi-blb2.Crossref | GoogleScholarGoogle Scholar | 19794118PubMed |
Park RF, Wellings CR, Bariana HS (2007) Preface to ‘global landscapes in cereal rust control’. Australian Journal of Agricultural Research 58, 469
| Preface to ‘global landscapes in cereal rust control’.Crossref | GoogleScholarGoogle Scholar |
Pogue GP, Lindbo JA, Dawson WO, Turpen TH (1998) Tobamovirus transient expression vectors: tools for plant biology and high-level expression of foreign proteins in plants. In ‘Plant molecular biology manual’. pp. 67–93. (Springer: Dordrecht, The Netherlands)
Roelfs AP, Martell LB (1984) Uredospore dispersal from a point source within a wheat canopy. Phytopathology 74, 1262–1267.
| Uredospore dispersal from a point source within a wheat canopy.Crossref | GoogleScholarGoogle Scholar |
Ryan CA (1987) Oligosaccharide signalling in plants. Annual Review of Cell Biology 3, 295–317.
| Oligosaccharide signalling in plants.Crossref | GoogleScholarGoogle Scholar | 3318878PubMed |
Saikia R, Singh BP, Kumar R (2005) Detection of pathogenesis-related proteins-chitinase and β-1,3-glucanase in induced chickpea. Current Science 89, 659–663.
Scofield SR, Huang L, Brandt AS, Gill BS (2005) Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiology 138, 2165–2173.
| Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway.Crossref | GoogleScholarGoogle Scholar | 16024691PubMed |
Shiferaw B, Smale M, Braun HJ, Duveiller E, Reynolds M, Muricho G (2013) Crops that feed the world 10. Past successes and future challenges to the role played by wheat in global food security. Food Security 5, 291–317.
| Crops that feed the world 10. Past successes and future challenges to the role played by wheat in global food security.Crossref | GoogleScholarGoogle Scholar |
Sundaresha S, Manoj KA, Rohini S, Math SA, Keshamma E, Chandrashekar SC (2010) Enhanced protection against two major fungal pathogens of groundnut, Cercospora arachidicola and Aspergillus flavus in transgenic groundnut over-expressing a tobacco β,1–3 glucanase. European Journal of Plant Pathology 126, 497–508.
| Enhanced protection against two major fungal pathogens of groundnut, Cercospora arachidicola and Aspergillus flavus in transgenic groundnut over-expressing a tobacco β,1–3 glucanase.Crossref | GoogleScholarGoogle Scholar |
Tian M, Win J, Savory E, Burkhardt A, Held M, Brandizzi F (2011) 454 Genome sequencing of Pseudoperonospora cubensis reveals effector proteins with a QXLR translocation motif. Molecular Plant-Microbe Interactions 24, 543
| 454 Genome sequencing of Pseudoperonospora cubensis reveals effector proteins with a QXLR translocation motif.Crossref | GoogleScholarGoogle Scholar | 21261462PubMed |
Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J (1992) Acquired resistance in Arabidopsis. The Plant Cell 4, 645–656.
Wang CF, Huang LL, Buchenauer H, Han QM, Zhang HC, Kang ZS (2007) Histochemical studies on the accumulation of reactive oxygen species (O2– and H2O2) in the incompatible and compatible interaction of wheat-Puccinia striiformis, f. sp. tritici. Physiological and Molecular Plant Pathology 71, 230–239.
| Histochemical studies on the accumulation of reactive oxygen species (O2– and H2O2) in the incompatible and compatible interaction of wheat-Puccinia striiformis, f. sp. tritici.Crossref | GoogleScholarGoogle Scholar |
Wang B, Sun Y, Song N, Zhao M, Liu R, Feng H, Wang X, Kang Z (2017) Puccinia striiformis f. sp. tritici microRNA-like RNA 1 (Pst-milR1), an important pathogenicity factor of pst, impairs wheat resistance to pst by suppressing the wheat pathogenesis-related 2 gene. New Phytologist 215, 338–350.
Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Metraux JP, Ryals JA (1991) Coordinat gene activity in response to agents that induce systemic acquired resistance. The Plant Cell 3, 1085–1094.
| Coordinat gene activity in response to agents that induce systemic acquired resistance.Crossref | GoogleScholarGoogle Scholar | 12324583PubMed |
Zhang J, Wang F, Liang F, Zhang Y, Ma L, Wang H, Liu D (2018) Functional analysis of a pathogenesis-related thaumatin-like protein gene TaLr35PR5 from wheat induced by leaf rust fungus. BMC Plant Biology 18, 76
| Functional analysis of a pathogenesis-related thaumatin-like protein gene TaLr35PR5 from wheat induced by leaf rust fungus.Crossref | GoogleScholarGoogle Scholar | 29728059PubMed |
Zhen XH, Li YZ (2004) Ultrastructural changes and location of β-1,3-glucanase in resistant and susceptible cotton callus cells in response to treatment with toxin of Verticillium dahliae and salicylic acid. Journal of Plant Physiology 161, 1367–1377.
| Ultrastructural changes and location of β-1,3-glucanase in resistant and susceptible cotton callus cells in response to treatment with toxin of Verticillium dahliae and salicylic acid.Crossref | GoogleScholarGoogle Scholar | 15658807PubMed |
