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Two Indigenous Berberis Species From Spain Were Confirmed as Alternate Hosts of the Yellow Rust Fungus Puccinia striiformis f. sp. tritici

^†Corresponding author: J. Rodriguez-Algaba;

E-mail Address: julianr.algaba@agro.au.dk

Global Rust Reference Center, Department of Agroecology, Faculty of Science and Technology, Aarhus University, Forsøgsvej 1, 4200 Slagelse, Denmark

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M. S. Hovmøller

Global Rust Reference Center, Department of Agroecology, Faculty of Science and Technology, Aarhus University, Forsøgsvej 1, 4200 Slagelse, Denmark

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D. Villegas

IRTA, Institute for Food and Agricultural Research and Technology, 25198 Lleida, Spain

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C. Cantero-Martínez

University of Lleida, Agrotecnio, 25198 Lleida, Spain

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Y. Jin

U.S. Department of Agriculture-Agricultural Research Service, Cereal Disease Laboratory, University of Minnesota, St. Paul, MN 55108, U.S.A.

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, and

A. F. Justesen

Global Rust Reference Center, Department of Agroecology, Faculty of Science and Technology, Aarhus University, Forsøgsvej 1, 4200 Slagelse, Denmark

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Affiliations

Authors and Affiliations

J. Rodriguez-Algaba¹^†
M. S. Hovmøller¹
D. Villegas²
C. Cantero-Martínez³
Y. Jin⁴
A. F. Justesen¹

¹Global Rust Reference Center, Department of Agroecology, Faculty of Science and Technology, Aarhus University, Forsøgsvej 1, 4200 Slagelse, Denmark
²IRTA, Institute for Food and Agricultural Research and Technology, 25198 Lleida, Spain
³University of Lleida, Agrotecnio, 25198 Lleida, Spain
⁴U.S. Department of Agriculture-Agricultural Research Service, Cereal Disease Laboratory, University of Minnesota, St. Paul, MN 55108, U.S.A.

Published Online:28 Oct 2021https://doi.org/10.1094/PDIS-02-21-0269-SC

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Abstract

Puccinia striiformis f. sp. tritici, which causes yellow (or stripe) rust on wheat, is a macrocyclic and heteroecious fungus. In this study, we investigated whether Berberis vulgaris subsp. seroi and B. vulgaris subsp. australis, which are indigenous in Spain, may serve as alternate hosts for P. striiformis f. sp. tritici. Wheat leaves bearing telia of an isolate of P. striiformis f. sp. tritici were harvested and used to inoculate plants of both barberry subspecies. Pycnia were observed on the adaxial side of the leaves from 10 days after inoculation (dai). Following successful fertilization, aecia were observed on the abaxial side of the leaves from 16 dai. At 27 dai, barberry leaves bearing aecia were detached and used to inoculate susceptible wheat seedlings of cultivar Morocco. Uredinia were observed on wheat seedlings from 12 days after aeciospore exposure. Eighty-three single lesions were recovered from individual wheat leaves, of which 43 were genotyped using 19 P. striiformis f. sp. tritici simple sequence repeat markers (SSR). In total, 19 multilocus genotypes (MLGs) were identified among the 43 progeny isolates. The SSR genotyping confirmed that all 43 isolates were derived from the parental isolate. Seven heterozygous SSR markers showed segregation among the progenies, whereas none of the 12 homozygous markers resulted in segregation. These results demonstrated that B. vulgaris subspp. seroi and australis can serve as alternate hosts for P. striiformis f. sp. tritici, which may result in novel virulence combinations that can have a detrimental impact on wheat production. Although P. striiformis f. sp. tritici has not been detected on these barberry species in nature, this study highlights the importance of rust surveillance in barberry areas where suitable conditions for completion of the sexual life cycle may be present.

Literature Cited

Ahrendt, L. W. A. 1961. Berberis and Mahonia. A taxonomic revision. J. Linn. Soc. (Bot.) 57. Google Scholar
Ali, S., Leconte, M., Walker, A. S., Enjalbert, J., and de Vallavieille-Pope, C. 2010. Reduction in the sex ability of worldwide clonal populations of Puccinia striiformis f. sp. tritici. Fungal Genet. Biol. 47:828-838. https://doi.org/10.1016/j.fgb.2010.07.002 Crossref, ISI, Google Scholar
Ali, S., Rodriguez-Algaba, J., Thach, T., Sørensen, C. K., Hansen, J. G., Lassen, P., Nazari, K., Hodson, D. P., Justesen, A. F., and Hovmøller, M. S. 2017. Yellow rust epidemics worldwide were caused by pathogen races from divergent genetic lineages. Front. Plant Sci. 8:1057. https://doi.org/10.3389/fpls.2017.01057 Crossref, ISI, Google Scholar
Barnes, G., Saunders, D. G. O., and Williamson, T. 2020. Banishing barberry: The history of Berberis vulgaris prevalence and wheat stem rust incidence across Britain. Plant Pathol. 69:1193-1202. https://doi.org/10.1111/ppa.13231 Crossref, ISI, Google Scholar
Beddow, J. M., Pardey, P. G., Chai, Y., Hurley, T. M., Kriticos, D. J., Braun, H. J., Park, R. F., Cuddy, W. S., and Yonow, T. 2015. Research investment implications of shifts in the global geography of wheat stripe rust. Nat. Plants 1:15132. https://doi.org/10.1038/nplants.2015.132 Crossref, ISI, Google Scholar
Berlin, A., Djurle, A., Samils, B., and Yuen, J. 2012. Genetic variation in Puccinia graminis collected from oats, rye, and barberry. Phytopathology 102:1006-1012. https://doi.org/10.1094/PHYTO-03-12-0041-R Link, ISI, Google Scholar
Hermansen, J. E. 1968. Studies on the spread and survival of cereal rust and mildew diseases in Denmark. The Royal Veterinary and Agricultural University, Copenhagen, Denmark. Google Scholar
Hovmøller, M. S., Walter, S., Bayles, R. A., Hubbard, A., Flath, K., Sommerfeldt, N., Leconte, M., Czembor, P., Rodriguez-Algaba, J., Thach, T., Hansen, J. G., Lassen, P., Justesen, A. F., Ali, S., and de Vallavieille-Pope, C. 2016. Replacement of the European wheat yellow rust population by new races from the centre of diversity in the near-Himalayan region. Plant Pathol. 65:402-411. https://doi.org/10.1111/ppa.12433 Crossref, ISI, Google Scholar
Jin, Y., Szabo, L. J., and Carson, M. 2010. Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternate host. Phytopathology 100:432-435. https://doi.org/10.1094/PHYTO-100-5-0432 Link, ISI, Google Scholar
Kamvar, Z. N., Tabima, J. F., and Grunwald, N. J. 2014. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281. https://doi.org/10.7717/peerj.281 Crossref, ISI, Google Scholar
Kim, Y. D., Kim, S. H., and Landrum, L. R. 2004. Taxonomic and phytogeographic implications from ITS phylogeny in Berberis (Berberidaceae). J. Plant Res. 117:175-182. https://doi.org/10.1007/s10265-004-0145-7 Crossref, ISI, Google Scholar
Kosalec, I., Gregurek, B., Kremer, D., Zovko, M., Sankovic, K., and Karlovic, K. 2009. Croatian barberry (Berberis croatica Horvat): a new source of berberine—analysis and antimicrobial activity. World J. Microbiol. Biotechnol. 25:145-150. https://doi.org/10.1007/s11274-008-9860-x Crossref, ISI, Google Scholar
Li, S., Chen, W., Ma, X., Tian, X., Liu, Y., Huang, L., Kang, Z., and Zhao, J. 2020. Identification of eight Berberis species from the Yunnan-Guizhou plateau as aecial hosts for Puccinia striiformis f. sp. tritici, the wheat stripe rust pathogen. J. Integr. Agric. 19:2-8. Google Scholar
López González, G. 1986. Berberidaceae. Pages 402-405 in: Flora Iberica, vol. 1. G. López González, ed. Real Jardín Botánico, CSIC, Madrid, Spain. Google Scholar
Mehmood, S., Sajid, M., Zhao, J., Huang, L., and Kang, Z. 2020. Alternate hosts of Puccinia striiformis f. sp. tritici and their role. Pathogens 9:434. https://doi.org/10.3390/pathogens9060434 Crossref, ISI, Google Scholar
Rodriguez-Algaba, J., Hovmøller, M. S., and Justesen, A. F. 2020. Sexual recombination within the “Kranich” race of the yellow rust fungus Puccinia striiformis f. sp. tritici on Berberis vulgaris. Eur. J. Plant Pathol. 156:1169-1173. https://doi.org/10.1007/s10658-019-01919-4 Crossref, ISI, Google Scholar
Rodriguez-Algaba, J., Sørensen, C. K., Labouriau, R., Justesen, A. F., and Hovmøller, M. S. 2017. Genetic diversity within and among aecia of the wheat rust fungus Puccinia striiformis on the alternate host Berberis vulgaris. Fungal Biol. 121:541-549. https://doi.org/10.1016/j.funbio.2017.03.003 Crossref, ISI, Google Scholar
Rodriguez-Algaba, J., Walter, S., Sorensen, C. K., Hovmoller, M. S., and Justesen, A. F. 2014. Sexual structures and recombination of the wheat rust fungus Puccinia striiformis on Berberis vulgaris. Fungal Genet. Biol. 70:77-85. https://doi.org/10.1016/j.fgb.2014.07.005 Crossref, ISI, Google Scholar
Roelfs, A. P. 1982. Effects of barberry eradication on stem rust in the United States. Plant Dis. 66:177-181. https://doi.org/10.1094/PD-66-177 Crossref, ISI, Google Scholar
Roelfs, A. P., and Groth, V. J. 1980. A comparison of virulence phenotypes in wheat stem rust populations reproducing sexually and asexually. Phytopathology 70:855-862. https://doi.org/10.1094/Phyto-70-855 Crossref, ISI, Google Scholar
Singh, R. P., Singh, P. K., Rutkoski, J., Hodson, D. P., He, X., Jorgensen, L. N., Hovmoller, M. S., and Huerta-Espino, J. 2016. Disease impact on wheat yield potential and prospects of genetic control. Annu. Rev. Phytopathol. 54:303-322. https://doi.org/10.1146/annurev-phyto-080615-095835 Crossref, ISI, Google Scholar
Stakman, E. C. 1923. Barberry eradication prevents black rust in Western Europe. United States Department of Agriculture, Washington, DC. Google Scholar
Stubbs, R. W. 1985. Stripe rust. Pages 61-101 in: The Cereal Rusts Vol. II: Diseases, Distribution, Epidemiology, and Control. A. P. Roelfs and W. R. Bushnell, eds. Academic Press, Orlando, FL. Crossref, Google Scholar
Wang, M. N., and Chen, X. M. 2013. First report of Oregon grape (Mahonia aquifolium) as an alternate host for the white stripe rust pathogen (Puccinia striiformis f. sp. tritici) under artificial inoculation. Plant Dis. 97:839. https://doi.org/10.1094/PDIS-09-12-0864-PDN Link, ISI, Google Scholar
Wang, M. N., Wan, A. M., and Chen, X. M. 2015. Barberry as alternate host is important for Puccinia graminis f. sp. tritici but not for Puccinia striiformis f. sp. tritici in the U.S. Pacific Northwest. Plant Dis. 99:1507-1516. https://doi.org/10.1094/PDIS-12-14-1279-RE Link, ISI, Google Scholar
Wang, Z., Zhao, J., Chen, X., Peng, Y., Ji, J., Zhao, S., Lv, Y., Huang, L., and Kang, Z. 2016. Virulence variations of Puccinia striiformis f. sp. tritici isolates collected from Berberis spp. in China. Plant Dis. 100:131-138. https://doi.org/10.1094/PDIS-12-14-1296-RE Link, ISI, Google Scholar
Zhao, J., Wang, L., Wang, Z., Chen, X., Zhang, H., Yao, J., Zhan, G., Chen, W., Huang, L., and Kang, Z. 2013. Identification of eighteen Berberis species as alternate hosts of Puccinia striiformis f. sp. tritici and virulence variation in the pathogen isolates from natural infection of barberry plants in China. Phytopathology 103:927-934. https://doi.org/10.1094/PHYTO-09-12-0249-R Link, ISI, Google Scholar
Zhao, J., Wang, M., Chen, X., and Kang, Z. 2016. Role of alternate hosts in epidemiology and pathogen variation of cereal rusts. Annu. Rev. Phytopathol. 54:207-228. https://doi.org/10.1146/annurev-phyto-080615-095851 Crossref, ISI, Google Scholar

Vol. 105, No. 9
September 2021

ISSN:0191-2917
e-ISSN:1943-7692

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Caption

Kadsura coccinea showing leaf spot caused by Botryosphaeria dothidea (D. Su et al.). Photo credit: D. Su. Leaf spot caused by Ramularia coleosporii on Perilla (M. Aktaruzzaman et al.). Photo credit: B. S. Kim. Injection inoculated maize plant showing a classification standard for maize stalk rot (W. Y. Jiang et al.). Photo credit: Y. G. Li.

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Article History

Issue Date: 8 Dec 2021
Published: 28 Oct 2021
First Look: 25 Feb 2021
Accepted: 20 Feb 2021

Pages: 2281-2285

Information

Funding

European Commission, Research and Innovation, Horizon 2020-Sustainable Food Security
Grant/Award Number: 773311-2

Bill and Melinda Gates Foundation (Delivering Genetic Gain in Wheat, DGGW)

Keywords

The author(s) declare no conflict of interest.