Skip to main content
Log in

Basidiospores of Puccinia striiformis f. sp. tritici succeed to infect barberry, while Urediniospores are blocked by non-host resistance

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Stripe rust (Yellow rust) caused by Puccinia striiformis f. sp. tritici (Pst) is a major disease of wheat worldwide. The use of resistant cultivars to control Pst has been very effective, low-cost, and ecologically sound. However, virulence patterns of Pst can quickly change, which may render resistant cultivars susceptible. The discovery of infection of Berberis spp. by basidiospores of Pst in 2010 raised important concerns about the evolution of new virulent races of the pathogen. Little is known about the infection process of Berberis spp. by basidiospores of Pst and the interaction between Berberis spp. and asexual urediniospores. In this study, the interaction between Pst urediniospores and Berberis spp. was investigated at histological and cytological levels. Our results indicate that Berberis spp. expresses a continuum of layered defenses comprised of structural and chemical changes in the cell wall as well as post-haustorial hypersensitive responses to urediniospore infection. Our study also re-examines in detail the infection process of Pst basidiospores on Berberis spp. and provides useful information for further research on the molecular mechanisms governing the interaction between Berberis spp. and Pst.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allen EA, Hoch HC, Steadman JR, Stavely RJ (1991) In: Andrews JH, Hirano SS (eds) “Influence of leaf surface features on spore deposition and the epiphytic growth of phytopathogenic fungi”, in microbial ecology of leaves. Springer Verlag, New York, pp 87–110

    Google Scholar 

  • Apostol I, Heinstein PF, Low PS (1989) Rapid stimulation of an oxidative burst during elicitation of cultured plant cells role in defense and signal transduction. Plant Physiol 90:109–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ayliffe M, Devilla R, Mago R, White R, Talbot M, Pryor A, Leung H (2011) Nonhost resistance of rice to rust pathogens. Mol Plant-Microbe Interact 24:1143–1155

    Article  CAS  PubMed  Google Scholar 

  • Bux H, Rasheed A, Siyal MA, Kazi AG, Napar AA, Mujeeb-Kazi A (2012) An overview of stripe rust of wheat (Puccinia striiformis f. sp. tritici) in Pakistan. Arch Phytopathol Plant Protec 45:2278–2289

    Article  Google Scholar 

  • Chen X (2005) Epidemiology and control of stripe rust (Puccinia striiformis f. sp. tritici) on wheat. Can J Plant Pathol 27:314–337

    Article  Google Scholar 

  • Cheng Y, Zhang H, Yao J, Han Q, Wang X, Huang L, Kang Z (2013) Cytological and molecular characterization of non-host resistance in Arabidopsis thaliana against wheat stripe rust. Plant Physiol Bioch 62:11–18

    Article  CAS  Google Scholar 

  • Cheng Y, Zhang H, Yao J, Wang X, Xu J, Han Q, Wei G, Huang L, Kang Z (2012) Characterization of non-host resistance in broad bean to the wheat stripe rust pathogen. BMC Plant Biol 12:96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430

    Article  PubMed  Google Scholar 

  • Gold RE, Mendgen K (1984) Cytology of basidiospore germination, penetration, and early colonization of Phaseolus vulgaris by Uromyces appendiculatus var. appendiculatus. Can J Bot 62:1989–2002

    Article  Google Scholar 

  • Gray D, Amerson H, Van Dyke C (1983) Ultrastructure of the infection and early colonization of Pinus taeda by Cronartium quercuum formae speciales fusiforme. Mycologia 75:117–130

    Article  Google Scholar 

  • Heath MC (1974) Light and electron microscope studies of the interactions of host and non-host plants with cowpea rust-Uromyces phaseoli var. vignae. Physiol. Plant Pathol 4:403–414

    Google Scholar 

  • Heath MC (1979) Partial characterization of the electron-opaque deposits formed in the non-host plant, French bean, after cowpea rust infection. Physiol Plant Pathol 15:141–148

    Article  Google Scholar 

  • Hood M, Shew H (1996) Applications of KOH-aniline blue fluorescence in the study of plant-fungal interactions. Phytopathology 86:704–708

    Article  Google Scholar 

  • Hoogkamp T, Chen WQ, Niks R (1998) Specificity of prehaustorial resistance to Puccinia hordei and to two inappropriate rust fungi in barley. Phytopathology 88:856–861

    Article  CAS  PubMed  Google Scholar 

  • Jacobi W, Amerson H, Mott R (1982) Microscopy of cultured loblolly pine seedlings and callus inoculated with Cronartium fusiforme. Phytopathology 72:138–143

    Article  Google Scholar 

  • Jin Y (2011) Role of Berberis spp. as alternate hosts in generating new races of Puccinia graminis and P. striiformis. Euphytica 179:105–108

    Article  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Kang Z, Huang L, Buchenauer H (2002) Ultrastructural changes and localization of lignin and callose in compatible and incompatible interactions between wheat and Puccinia striiformis. J Plant Dis Prot 109:25–37

    CAS  Google Scholar 

  • Koch K, Bhushan B, Barthlott W (2009) Multifunctional surface structures of plants: an inspiration for biomimetics. Prog Mater Sci 54:137–178

    Article  CAS  Google Scholar 

  • Kohno M, Nishimura T, Noda M, Ishizaki H, Kunoh H (1977) Cytological studies on rust fungi. (VII) The nuclear behavior of Gymnosporangium asiaticum Miyabe et Yamada during the stages from teliospore germination through sporidium germination. Transac Mycol Soc Jap 18:211–219

    Google Scholar 

  • Lipka U, Fuchs R, Lipka V (2008) Arabidopsis non-host resistance to powdery mildews. Curr Opin Plant Biol 11:404–411

    Article  CAS  PubMed  Google Scholar 

  • Metzler B (1982) Untersuchungen an Heterobasidiomyceten (23): Basidiosporenkeimung und Infektionsvorgang beim Birnengitterrost. Phytopathol Z 103:126–138

    Google Scholar 

  • Mims CW (1977) Fine structure of basidiospores of the cedar-apple rust fungus Gymnosporangium juniperi-virginianae. Can J Bot 55:1057–1063

    Article  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Niks R (1982) Early abortion of colonies of leaf rust, Puccinia hordei, in partially resistant barley seedlings. Can J Bot 60:714–723

    Article  Google Scholar 

  • Niks R (1983a) Comparative histology of partial resistance and the nonhost reaction to leaf rust pathogens in barley and wheat seedlings. Phytopathology 73:60–64

    Article  Google Scholar 

  • Niks R (1983b) Haustorium formation by Puccinia hordei in leaves of hypersensitive, partially resistant, and nonhost plant genotypes. Phytopathology 73:64–66

    Article  Google Scholar 

  • Nusbaum CJ (1935) A cytological study of the resistance of apple varieties to Gymnosporangium juniperi-virginianae. J Agric Res 51:573–596

    Google Scholar 

  • Schulze-Lefert P, Panstruga R (2011) A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci 16:117–125

    Article  CAS  PubMed  Google Scholar 

  • Thordal-Christensen H (2003) Fresh insights into processes of nonhost resistance. Curr Opin Plant Biol 6:351–357

    Article  CAS  PubMed  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Voegele RT, Struck C, Hahn M, Mendgen K (2001) The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Nat Acad Sci USA 98:8133–8138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Physiol Mol Plant Pathol 71:230–239

    Article  CAS  Google Scholar 

  • Wang CF, Huang LL, Zhang HC, Han QM, Buchenauer H, Kang ZS (2010) Cytochemical localization of reactive oxygen species (O2− and H2O2) and peroxidase in the incompatible and compatible interaction of wheat–Puccinia striiformis f. sp. tritici. Physiol Mol Plant Pathol 74:221–229

    Article  CAS  Google Scholar 

  • Yang Y, Zhao J, Xing H, Wang J, Zhou K, Zhan G, Zhang H, Kang Z (2014) Different non-host resistance responses of two rice subspecies, japonica and indica, to Puccinia striiformis f. sp. tritici. Plant Cell Rep 33:423–433

    Article  PubMed  Google Scholar 

  • Zhang H, Wang C, Cheng Y, Chen X, Han Q, Huang L, Wei G, Kang Z (2012) Histological and cytological characterization of adult plant resistance to wheat stripe rust. Plant Cell Rep 31:2121–2137

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Wang L, Wang Z, Chen X, Zhang H, Yao J, Zhan G, Chen W, Huang L, 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

    Article  PubMed  Google Scholar 

  • Zhao J, Zhang HC, Yao JN, Huang LL, Kang ZS (2011) Confirmation of Berberis spp. as alternate hosts of Puccinia striiformis f. sp. tritici on wheat in China. Mycosystema 30:895–900

    CAS  Google Scholar 

Download references

Acknowledgements

This study has been financially supported by the National Key Basic Research Program of China (2013CB127700), the National Natural Science Foundation of China (31371889), Research Fund for the Doctoral program of Higher Education of China (20130204110001), the Program for New Century Excellent Talents in University (NCET-12-0471), and the 111 Project from the Ministry of Education of China (B07049). The authors thank Professor Larry Dunkle from the USDA-Agricultural Research Service at Purdue University, USA, for critical reading of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

JuG and ZK designed experiments; MJ performed the experiments; CT and LW analyzed the data; HZ and JiG joined the discussion and gave the original ideas; and MJ, JuG, and ZK wrote the paper.

Corresponding authors

Correspondence to Zhensheng Kang or Jun Guo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest

Additional information

Handling Editor: Adrienne R. Hardham

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiao, M., Tan, C., Wang, L. et al. Basidiospores of Puccinia striiformis f. sp. tritici succeed to infect barberry, while Urediniospores are blocked by non-host resistance. Protoplasma 254, 2237–2246 (2017). https://doi.org/10.1007/s00709-017-1114-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-017-1114-z

Keywords

Navigation