Abstract
Main conclusion
We report the first comparative study of protein expression profiles in tuber sprouts between Katahdin-derived potato cultivars resistant and susceptible to Synchytrium endobioticum.
Abstract
Synchytrium endobioticum causes wart disease in potato (Solanum tuberosum L.) and is considered as the most important quarantine pathogen in almost all countries where potatoes are grown. We performed a comparative analysis of differentially expressed proteins in the tuber sprouts of potato cultivars differing in resistance to pathotype 1(D1) of S. endobioticum using two-dimensional electrophoresis (2-DE) and liquid chromatography–tandem mass spectrometry (LC–MS/MS) approaches. Bulks prepared from two resistant (Calrose and Humalda) and three susceptible (Sebago, Seneca and Wauseon) potato cultivars were studied. When protein profiles were compared between mock- and S. endobioticum-inoculated sprouts, 35 and 63 protein spots, indicating qualitative or quantitative differences, were detected in the resistant and susceptible cultivars, respectively. In turn, 24 proteins associated with resistance to S. endobioticum were revealed by comparison of the resistant and susceptible bulks. These proteins were changed in a constitutive or induced manner and were grouped into four categories: stress and defence, cell structure, protein turnover, and metabolism. Among the 13 proteins classified into the stress and defence group, seven proteins were related to heat-shock proteins (HSPs)/chaperone factors. In addition, four proteins, S-adenosyl-l-homocysteine hydrolase-like, superoxide dismutase [Mn], inactive patatin-3-Kuras 1 and patatin-15, were induced in the resistant bulk; whereas two proteins, patatin-01 and nucleoredoxin 1, showed significant differences in expression between the S. endobioticum-inoculated resistant and susceptible bulks. The detection of such a large number of S. endobioticum-mediated proteins representing the HSP70, HSP60 and HSP20 families suggests their significant role in restricting wart disease in potato tubers.
References
Ali A, Alexandersson E, Sandin M, Resjö S, Lenman M, Hedley P, Levander F, Andreasson E (2014) Quantitative proteomics and transcriptomics of potato in response to Phytophthora infestans in compatible and incompatible interactions. BMC Genom 15:497
Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Gzyl J, Chmielowska-Bąk J (2013) Homocysteine over-accumulation as the effect of potato leaves exposure to biotic stress. Plant Physiol 63:177–184
Baayen R, Cochius G, Hendriks H, Meffert J, Bakker J, Bekker M, van den Boogert P, Stachewicz H, van Leeuwen G (2006) History of potato wart disease in Europe—a proposal for harmonization in defining pathotypes. Eur J Plant Pathol 116:21–31
Baebler S, Krecic-Stres H, Rotter A, Kogovšek P, Cankar K, Kok EJ et al (2009) PVYNTN elicits a diverse gene expression response in different potato genotypes in the first 12 h after inoculation. Mol Plant Pathol 10:263–275
Bárta J, Bártowá V (2008) Patatin, the major protein of potato (Solanum tuberosum L.) tubers, and its occurrence as genotype effect: processing versus table potatoes. Czech J Food Sci 26:347–359
Cakir E, van Leeuwen GCM, Flath K, Meffert JP, Janssen WAP, Maden S (2009) Identification of pathotypes of Synchytrium endobioticum found in infested fields in Turkey. OEPP EPPO Bull 39:175–178
Clark CF, Stuart W, Stevenson FJ (1931) The Katahdin potato: a new variety. Am Potato J 8:121–125
Doke N (1985) NADPH-dependent O2 generation in membrane fractions isolated from wounded potato tubers inoculated with Phytophthora infestans. Physiol Plant Pathol 27:311–322
Fang X, Chen J, Dai L, Ma H, Zhang H, Yang J, Wang F, Chengqi Y (2015) Proteomic dissection of plant responses to various pathogens. J Proteomics 15:1525–1543
González-Fernández R, Prats E, Jorrín-Novo JV (2010) Proteomics of plant pathogenic fungi. J Biomed Biotechnol. https://doi.org/10.1155/2010/932527(Art. ID 932527)
Hampson MC (1993) History, biology and control of potato wart disease in Canada. Can J Plant Pathol 15:223–244
Hehl R, Faurie E, Hesselbach J, Salamini F, Whitham S, Baker B, Gebhardt C (1999) TMV resistance gene N homologues are linked to Synchytrium endobioticum resistance in potato. Theor Appl Genet 98:379–386
Jacob P, Hirt H, Bendahmane A (2017) The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotechnol J 15:405–414
Kneeshaw S, Keyani R, Delorme-Hinoux V, Imrie L, Loake GJ, Le Bihan T, Reichheld J-P, Spoel SH (2017) Nucleoredoxin guards against oxidative stress by protecting antioxidant enzymes. Proc Natl Acad Sci USA 114:8414–8419
La Camera S, Geoffroy P, Samaha H, Ndiaye A, Rahim G, Legrand M, Heitz T (2005) A pathogen-inducible patatin-like lipid acyl hydrolase facilitates fungal and bacterial host colonization in Arabidopsis. Plant J 44:810–825
Lellbach H, Effmert M (1990) Results of diallel analysis of the genetics of resistance to Synchytrium endobioticum (Schilb.) Perc., pathotype 1(D1) of potato (Solanum tuberosum L.). Potato Res 33:251–256
Liu J, Pang X, Cheng Y, Yin Y, Zhang Q, Su W, Hu B, Guo Q, Ha S, Zhang J, Wan H (2018) The Hsp70 gene family in Solanum tuberosum: genome-wide identification, phylogeny, and expression patterns. Sci Rep 8:16628
Makarova S, Makhotenko A, Spechenkova N, Love AJ, Kalinina N, Taliansky M (2018) Interactive responses of potato (Solanum tuberosum L.) plants to heat stress and infection with Potato Virus Y. Front Microbiol 9:2582
Melnik PA (1998) Wart disease of potato, Synchytrium endobioticum (Schilbersky) Percival. Paris: EPPO Technical documents 1032
Park Ch-J, Seo Y-S (2015) Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathol J 3:323–333
Plich J, Przetakiewicz J, Śliwka J, Flis B, Wasilewicz-Flis I, Zimnoch-Guzowska E (2018) Novel gene Sen2 conferring broad-spectrum resistance to Synchytrium endobioticum mapped to potato chromosome XI. Theor Appl Genet 131:2321–2331
Podgórska A, Burian M, Szal B (2017) Extra-cellular but extra-ordinarily important for cells: apoplastic reactive oxygen species metabolism. Front Plant Sci 8:1353
Przetakiewicz J (2015a) The viability of winter sporangia of Synchytrium endobioticum (Schilb.) Perc. from Poland. Am J Potato Res 92:704–708
Przetakiewicz J (2015b) First report of new pathotype 39(P1) of Synhytrium endobioticum causing potato wart disease in Poland. Plant Dis 99(285):2
Przetakiewicz J (2017) Sampling, maintenance and pathotype identification of Synchytrium endobioticum (Schilb.) Perc. Plant Breed Seed Sci 76:29–36
Przetakiewicz J, Plich J (2017) Assessment of potato resistance to Synchytrium endobioticum. Plant Breed Seed Sci 76:36–43
Resjö S, Brus M, Ali A, Meijer HJG, Sandin M, Govers F, Levander F, Grenville-Briggs L, Andreasson E (2017) Proteomic analysis of Phytophthora infestans reveals the importance of cell wall proteins in pathogenicity. Mol Cell Proteom 16:1958–1971
Senda K, Yoshioka H, Doke N, Kawakita K (1996) A cytosolic phospholipase A2 from potato tissues appears to be patatin. Plant Cell Physiol 37(3):347–353
Shewry PR (2003) Tuber storage proteins. Ann Bot 91:755–769
Soltys-Kalina D, Plich J, Strzelczyk-Żyta D, Śliwka J, Marczewski W (2016) The effect of drought stress on the leaf relative water content and tuber yield of a half-sib family of ‘Katahdin’-derived potato cultivars. Breed Sci 66:328–331
Szajko K, Strzelczyk-Żyta D, Marczewski W (2018) Comparison of leaf proteomes of potato (Solanum tuberosum L.) genotypes with ER- and HR-mediated resistance to PVY infection. Eur J Plant Pathol 150:375–385
USDA-APHIS (2002) Agricultural bioterrorism protection act 2002: listing of biological agents and requirements and procedures for notification of possession. Fed Reg 67:52283–52389
van de Vossenberg BTLH, Prodhomme C, van Arkel G, Marga PE, van Gent-Pelzer MPE, Bergervoet M, Brankovics B, Przetakiewicz J, Visser RGF, van der Lee TAJ, Vossen JH (2019) The Synchytrium endobioticum AvrSen1 triggers a hypersensitive response in Sen1 potatoes while natural variants evade detection. Mol Plant Microbe Interact. https://doi.org/10.1094/MPMI-05-19-0138-R
Vogel C, Marcotte EM (2012) Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet 13:227–232
Wu L, Han Z, Wang S, Wang X, Sun A, Zu X, Chen Y (2013) Comparative proteomic analysis of the plant–virus interaction in resistant and susceptible ecotypes of maize infected with sugarcane mosaic virus. J Proteome 89:124–140
Zhang X, Fu J, Hiromasa Y, Pan H, Bai G (2013) Differentially expressed proteins associated with Fusarium head blight resistance in wheat. PLoS One 8(12):e82079
Zou C, Wang P, Xu Y (2016) Bulked sample analysis in genetics, genomics and crop improvement. Plant Biotechnol J 14(10):1941–1955
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The research was supported by Polish Ministry of Science and Higher Education (project 1-3-00-1-01) and National Science Center in Poland (project No. 2013/11/B/NZ9/01959).
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Szajko, K., Plich, J., Przetakiewicz, J. et al. Comparative proteomic analysis of resistant and susceptible potato cultivars during Synchytrium endobioticum infestation. Planta 251, 4 (2020). https://doi.org/10.1007/s00425-019-03306-z
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DOI: https://doi.org/10.1007/s00425-019-03306-z