Abstract
Key message
The overexpression of rice BSR2 would offer a simple and effective strategy to protect plants from multiple devastating diseases in tomato and Arabidopsis.
Abstract
Many devastating plant diseases are caused by pathogens possessing a wide host range. Fungal Botrytis cinerea and Rhizoctonia solani, as well as bacterial Pseudomonas syringae and Ralstonia pseudosolanacearum are four such pathogens that infect hundreds of plant species, including agronomically important crops, and cause serious diseases, leading to severe economic losses. However, reports of genes that can confer resistance to broad host-range pathogens via traditional breeding methods are currently limited. We previously reported that Arabidopsis plants overexpressing rice BROAD-SPECTRUM RESISTANCE2 (BSR2/CYP78A15) showed tolerance not only to bacterial P. syringae pv. tomato DC3000 but also to fungal Colletotrichum higginsianum and R. solani. Rice plants overexpressing BSR2 displayed tolerance to two R. solani anastomosis groups. In the present study, first, BSR2-overexpressing (OX) Arabidopsis plants were shown to be additionally tolerant to B. cinerea, R. solani, and R. pseudosolanacearum. Next, tomato ‘Micro-Tom’ was used as a model to determine whether such tolerance by BSR2 can be introduced into dicot crops to prevent infection from pathogens possessing wide host range. BSR2-OX tomato displayed broad-spectrum disease tolerance to fungal B. cinerea and R. solani, as well as to bacterial P. syringae and R. pseudosolanacearum. Additionally, undesirable traits such as morphological changes were not detected. Thus, BSR2 overexpression can offer a simple and effective strategy to protect crops from multiple destructive diseases.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adamski NM, Anastasiou E, Eriksson S, O'Neill CM, Lenhard M (2009) Local maternal control of seed size by KLUH/CYP78A5-dependent growth signaling. Proc Natl Acad Sci USA 106:20115–20120. https://doi.org/10.1073/pnas.0907024106
Anastasiou E, Kenz S, Gerstung M, MacLean D, Timmer J, Fleck C, Lenhard M (2007) Control of plant organ size by KLUH/CYP78A5-dependent intercellular signaling. Dev Cell 13:843–856. https://doi.org/10.1016/j.devcel.2007.10.001
Arnold DL, Preston GM (2019) Pseudomonas syringae: enterprising epiphyte and stealthy parasite. Microbiology 165:251–253. https://doi.org/10.1099/mic.0.000715
Asaka O, Shoda M (1996) Biocontrol of Rhizoctonia solani Damping-Off of Tomato with Bacillus subtilis RB14. Appl Environ Microbiol 62:4081–4085
Badejo AA, Wada K, Gao Y, Maruta T, Sawa Y, Shigeoka S, Ishikawa T (2012) Translocation and the alternative D-galacturonate pathway contribute to increasing the ascorbate level in ripening tomato fruits together with the D-mannose/L-galactose pathway. J Exp Bot 63:229–239. https://doi.org/10.1093/jxb/err275
Bishop GJ et al (1999) The tomato DWARF enzyme catalyses C-6 oxidation in brassinosteroid biosynthesis. Proc Natl Acad Sci USA 96:1761–1766. https://doi.org/10.1073/pnas.96.4.1761
Budge GE, Shaw MW, Colyer A, Pietravalle S, Boonham N (2009) Molecular tools to investigate Rhizoctonia solani distribution in soil. Plant Pathol 58:1071–1080. https://doi.org/10.1111/j.1365-3059.2009.02139.x
Carling DE, Baird RE, Gitaitis RD, Brainard KA, Kuninaga S (2002) Characterization of AG-13, a newly reported anastomosis group of Rhizoctonia solani. Phytopathology 92:893–899. https://doi.org/10.1094/PHYTO.2002.92.8.893
Chakrabarti M et al (2013) A cytochrome P450 regulates a domestication trait in cultivated tomato. Proc Natl Acad Sci USA 110:17125–17130. https://doi.org/10.1073/pnas.1307313110
Dean R et al (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430. https://doi.org/10.1111/j.1364-3703.2011.00783.x
Dubouzet JG et al (2011) Screening for resistance against Pseudomonas syringae in rice-FOX Arabidopsis lines identified a putative receptor-like cytoplasmic kinase gene that confers resistance to major bacterial and fungal pathogens in Arabidopsis and rice. Plant Biotechnol J 9:466–485. https://doi.org/10.1111/j.1467-7652.2010.00568.x
Fang W, Wang Z, Cui R, Li J, Li Y (2012) Maternal control of seed size by EOD3/CYP78A6 in Arabidopsis thaliana. Plant J 70:929–939. https://doi.org/10.1111/j.1365-313X.2012.04907.x
Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051. https://doi.org/10.1126/science.220.4601.1049
Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158. https://doi.org/10.1016/0014-4827(68)90403-5
Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16(Suppl):S170–180. https://doi.org/10.1105/tpc.019158
Gondal AS, Rauf A, Naz F (2019) Anastomosis groups of Rhizoctonia solani associated with tomato foot rot in Pothohar Region of Pakistan. Sci Rep 9:3910. https://doi.org/10.1038/s41598-019-40043-5
Guimaraes RL, Chetelat RT, Stotz HU (2004) Resistance to Botrytis cinerea in Solanum lycopersicoides is dominant in hybrids with tomato, and involves induced hyphal death. Eur J Plant Pathol 110:13–23. https://doi.org/10.1023/B:EJPP.0000010133.62052.e4
Hane JK, Anderson JP, Williams AH, Sperschneider J, Singh KB (2014) Genome sequencing and comparative genomics of the broad host-range pathogen Rhizoctonia solani AG8. PLoS Genet 10:e1004281. https://doi.org/10.1371/journal.pgen.1004281
Imaishi H, Matsuo S, Swai E, Ohkawa H (2000) CYP78A1 preferentially expressed in developing inflorescences of Zea mays encoded a cytochrome P450-dependent lauric acid 12-monooxygenase. Biosci Biotechnol Biochem 64:1696–1701
Ito T, Meyerowitz EM (2000) Overexpression of a gene encoding a cytochrome P450, CYP78A9, induces large and seedless fruit in arabidopsis. Plant Cell 12:1541–1550
Knapp S (2002) Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae. J Exp Bot 53:2001–2022. https://doi.org/10.1093/jxb/erf068
Ma M, Zhao H, Li Z, Hu S, Song W, Liu X (2016) TaCYP78A5 regulates seed size in wheat (Triticum aestivum). J Exp Bot 67:1397–1410. https://doi.org/10.1093/jxb/erv542
Maeda S et al (2019) The rice CYP78A gene BSR2 confers resistance to Rhizoctonia solani and affects seed size and growth in Arabidopsis and rice. Sci Rep 9:587. https://doi.org/10.1038/s41598-018-37365-1
Mansfield J et al (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13:614–629. https://doi.org/10.1111/j.1364-3703.2012.00804.x
Marti E, Gisbert C, Bishop GJ, Dixon MS, Garcia-Martinez JL (2006) Genetic and physiological characterization of tomato cv. Micro-Tom J Exp Bot 57:2037–2047. https://doi.org/10.1093/jxb/erj154
Misawa T, Kuninaga S (2010) The first report of tomato foot rot caused by Rhizoctonia solani AG-3 PT and AG-2-Nt and its host range and molecular characterization. J Gener Plant Pathol 76:310–319. https://doi.org/10.1007/s10327-010-0261-2
Miyoshi K, Ahn BO, Kawakatsu T, Ito Y, Itoh J, Nagato Y, Kurata N (2004) PLASTOCHRON1, a timekeeper of leaf initiation in rice, encodes cytochrome P450. Proc Natl Acad Sci USA 101:875–880. https://doi.org/10.1073/pnas.2636936100
Nagasawa N et al (2013) GIANT EMBRYO encodes CYP78A13, required for proper size balance between embryo and endosperm in rice. Plant J 75:592–605. https://doi.org/10.1111/tpj.12223
Nakagawa H et al (2012) Short grain1 decreases organ elongation and brassinosteroid response in rice. Plant Physiol 158:1208–1219. https://doi.org/10.1104/pp.111.187567
Rothan C, Diouf I, Causse M (2019) Trait discovery and editing in tomato. Plant J 97:73–90. https://doi.org/10.1111/tpj.14152
Sato Y et al (2013) RiceXPro version 3.0: expanding the informatics resource for rice transcriptome. Nucleic Acids Res 41:D1206–1213. https://doi.org/10.1093/nar/gks1125
Seo S et al (2012) Identification of natural diterpenes that inhibit bacterial wilt disease in tobacco, tomato and Arabidopsis. Plant Cell Physiol 53:1432–1444. https://doi.org/10.1093/pcp/pcs085
Shikata M, Ezura H (2016) Micro-Tom tomato as an alternative plant model system: mutant collection and efficient transformation. Methods Mol Biol 1363:47–55. https://doi.org/10.1007/978-1-4939-3115-6_5
Soltis NE et al (2019) Interactions of tomato and Botrytis cinerea genetic diversity: parsing the contributions of host differentiation, domestication, and pathogen variation. Plant Cell 31:502–519. https://doi.org/10.1105/tpc.18.00857
Sotelo-Silveira M, Cucinotta M, Chauvin AL, Chávez Montes RA, Colombo L, Marsch-Martínez N, de Folter S (2013) Cytochrome P450 CYP78A9 is involved in Arabidopsis reproductive development. Plant Physiol 162:779–799. https://doi.org/10.1104/pp.113.218214
Sun X et al (2017) Altered expression of maize PLASTOCHRON1 enhances biomass and seed yield by extending cell division duration. Nat Commun 8:14752. https://doi.org/10.1038/ncomms14752
Takahashi H et al (2005) Catalog of Micro-Tom tomato responses to common fungal, bacterial, and viral pathogens. J Gener Plant Pathol 71:8–22. https://doi.org/10.1007/s10327-004-0168-x
Tanaka A et al (2009) BRASSINOSTEROID UPREGULATED1, encoding a helix-loop-helix protein, is a novel gene involved in brassinosteroid signaling and controls bending of the lamina joint in rice. Plant Physiol 151:669–680. https://doi.org/10.1104/pp.109.140806
Wang X, Li Y, Zhang H, Sun G, Zhang W, Qiu L (2015) Evolution and association analysis of GmCYP78A10 gene with seed size/weight and pod number in soybean. Mol Biol Rep 42:489–496. https://doi.org/10.1007/s11033-014-3792-3
Wang JW, Schwab R, Czech B, Mica E, Weigel D (2008) Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20:1231–1243. https://doi.org/10.1105/tpc.108.058180
Williamson B, Tudzynski B, Tudzynski P, van Kan JA (2007) Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8:561–580. https://doi.org/10.1111/j.1364-3703.2007.00417.x
Xu F et al (2015) Variations in CYP78A13 coding region influence grain size and yield in rice. Plant Cell Environ 38:800–811. https://doi.org/10.1111/pce.12452
Yang W et al (2013) Control of rice embryo development, shoot apical meristem maintenance, and grain yield by a novel cytochrome p450. Mol Plant 6:1945–1960. https://doi.org/10.1093/mp/sst107
Yang G, Li C (2012) General description of rhizoctonia species complex. Plant Pathol 2012:41–52. https://doi.org/10.5772/39026
Yuan JS, Reed A, Chen F, Stewart CN Jr (2006) Statistical analysis of real-time PCR data. BMC Bioinformatics 7:85. https://doi.org/10.1186/1471-2105-7-85
Zhao B, Dai A, Wei H, Yang S, Wang B, Jiang N, Feng X (2016) Arabidopsis KLU homologue GmCYP78A72 regulates seed size in soybean. Plant Mol Biol 90:33–47. https://doi.org/10.1007/s11103-015-0392-0
Zondlo SC, Irish VF (1999) CYP78A5 encodes a cytochrome P450 that marks the shoot apical meristem boundary in Arabidopsis. Plant J 19:259–268
Acknowledgements
This work was supported by the Special Coordination Fund for Promoting Science and Technology (Japan Science and Technology Agency), by grants for the Research Program on Development of Innovative Technology (NARO Bio-oriented Technology Research Advancement Institution (Grant no. 29004A)), and by the JSPS KAKENHI Grant (no. JP20H02953). We especially thank Dr. Shigemi Seo (NIAS, Japan) for helping with infection by R. pseudosolanacearum. We thank Dr. Brian J. Staskawicz (UC Berkeley, USA) for providing Pst DC3000, Dr. Toyozo Sato (NIAS, Japan) for helping with B. cinerea culture, and Dr. Aya Akagi (NIAS, Japan) for helping with infection by B. cinerea. Thanks go to Dr. Takahito Nomura (Utsunomiya Univ., Japan) and Dr. Yoshiki Habu (NIAS, Japan) for helpful discussions. We also thank Lois Ishizaki, Tomiko Senba, Chiyoko Umeda, and Yuka Yamazaki (NIAS, Japan) for their support with overall technical assistance. We would like to thank Editage (www.editage.com) for English language editing.
Author information
Authors and Affiliations
Contributions
SM carried out the experimental work and contributed to the manuscript composition. NY and KO contributed to the generation of transgenic tomato. MM directed the research and contributed to the manuscript composition.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Neal Stewart.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Maeda, S., Yokotani, N., Oda, K. et al. Enhanced resistance to fungal and bacterial diseases in tomato and Arabidopsis expressing BSR2 from rice. Plant Cell Rep 39, 1493–1503 (2020). https://doi.org/10.1007/s00299-020-02578-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-020-02578-0