Geographical variations, prevalence, and molecular dynamics of fastidious phloem-limited pathogens infecting sugar beet across Central Europe
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
38954690
PubMed Central
PMC11218978
DOI
10.1371/journal.pone.0306136
PII: PONE-D-24-17314
Knihovny.cz E-zdroje
- MeSH
- Ascomycota genetika MeSH
- Beta vulgaris * mikrobiologie MeSH
- floém * mikrobiologie MeSH
- fylogeneze MeSH
- nemoci rostlin * mikrobiologie MeSH
- Phytoplasma * genetika patogenita izolace a purifikace MeSH
- prevalence MeSH
- zeměpis MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Evropa epidemiologie MeSH
In Europe, two fastidious phloem-limited pathogens, 'Candidatus Phytoplasma solani' (16SrXII-A) and 'Candidatus Arsenophonus phytopathogenicus', are associated with rubbery taproot disease (RTD) and syndrome basses richesses (SBR) of sugar beet, respectively. Both diseases can significantly reduce yield, especially when accompanied by root rot fungi. This study investigates the presence, geographic distribution and genetic traits of fastidious pathogens and the accompanying fungus, Macrophomina phaseolina, found on sugar beet across four geographically separated plains spanning seven countries in Central Europe. The survey revealed variable incidences of symptoms linked to these fastidious pathogens in the Pannonian and Wallachian Plains, sporadic occurrence in the North European Plain, and no symptomatic sugar beet in the Bohemian Plain. Molecular analyses unveiled the occurrence of both 'Ca. P. solani' and 'Ca. A. phytopathogenicus' throughout Central Europe, with a predominance of the phytoplasma. These fastidious pathogens were detected in all six countries surveyed within the Pannonian and Wallachian Plains, with only a limited presence of various phytoplasmas was found in the North European Plain, while no fastidious pathogens were detected in Bohemia, aligning with observed symptoms. While 16S rDNA sequences of 'Ca. P. solani' remained highly conserved, multi-locus characterization of two more variable loci (tuf and stamp) unveiled distinct variability patterns across the plains. Notably, the surprising lack of variability of tuf and stamp loci within Central Europe, particularly the Pannonian Plain, contrasted their high variability in Eastern and Western Europe, corresponding to epidemic and sporadic occurrence, respectively. The current study provides valuable insights into the genetic dynamics of 'Ca. P. solani' in Central Europe, and novel findings of the presence of 'Ca. A. phytopathogenicus' in five countries (Slovakia, Czech Republic, Austria, Serbia, and Romania) and M. phaseolina in sugar beet in Slovakia. These findings emphasize the need for further investigation of vector-pathogen(s)-plant host interactions and ecological drivers of disease outbreaks.
Department of Plant Physiology Faculty of Biology Adam Mickiewicz University Poznań Poland
Institute of Pesticides and Environmental Protection Belgrade Serbia
University of Belgrade Faculty of Agriculture Belgrade Serbia
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Richard-Molard M, Garraessus S, Malatesta G, Orny G, Valentin P, Lemaire O, et al.. Le syndrome des basses richesses-Investigations au champ et tentatives d’identification de l’agent pathogene et du vecteur. In: Proceedings of the 58th Congres de L’Institut International de Recherches Betteravieres, Bruxelles. 1995. p. 19–22.
Sémétey O, Bressan A, Richard-Molard M, Boudon-Padieu E. Monitoring of proteobacteria and phytoplasma in sugar beets naturally or experimentally affected by the disease syndrome ‘basses richesses’. Eur J Plant Pathol. 2007. Feb 1;117(2):187–96.
Schröder M, Rissler D, Schrameyer K. ‘Syndrome des basses richesses’(SBR)—erstmaliges ruftreten an zuckerrübe in Deutschland. J Kulturpflanzen. 2012;64(10):396.
Mahillon M, Groux R, Bussereau F, Brodard J, Debonneville C, Demal S, et al.. Virus yellows and syndrome “basses richesses” in Western Switzerland: A Dramatic 2020 Season Calls for Urgent Control Measures. Pathogens. 2022. Aug;11(8):885. doi: 10.3390/pathogens11080885 PubMed DOI PMC
Pocsai E, Boudron-Padieu E, Desque D, Gatineau F, Larrue J, Ember I, et al.. Occurrence of "low-sugar syndrom" disease of sugar beet in Hungary. Novenyvedelem Hungary. 2005;411.
Ćurčić Ž, Kosovac A, Stepanović J, Rekanović E, Kube M, Duduk B. Multilocus genotyping of ‘Candidatus Phytoplasma solani’ associated with rubbery taproot disease of sugar beet in the Pannonian Plain. Microorganisms. 2021. Sep 14;9(9):1950. doi: 10.3390/microorganisms9091950 PubMed DOI PMC
Ćurčić Ž, Stepanović J, Zübert C, Taški-Ajduković K, Kosovac A, Rekanović E, et al.. Rubbery taproot disease of sugar beet in Serbia associated with ‘Candidatus Phytoplasma solani’. Plant Dis. 2021. Feb;105(2):255–63. PubMed
Duduk B, Ćurčić Ž, Stepanović J, Böhm JW, Kosovac A, Rekanović E, et al.. Prevalence of a ‘Candidatus Phytoplasma solani’-related strain designated as new 16SrXII-P subgroup over ‘Candidatus Arsenophonus phytopathogenicus’ in sugar beet in eastern Germany. Plant Dis. 2023. Dec;107(12):3792–800. doi: 10.1094/PDIS-04-23-0613-RE PubMed DOI
Duduk N, Vico I, Kosovac A, Stepanović J, Ćurčić Ž, Vučković N, et al.. A biotroph sets the stage for a necrotroph to play: ‘Candidatus Phytoplasma solani’ infection of sugar beet facilitated Macrophomina phaseolina root rot. Front Microbiol. 2023. Apr 20;14:1164035. doi: 10.3389/fmicb.2023.1164035 PubMed DOI PMC
Pfitzer R, Schrameyer K, Voegele RT, Maier J, Lang C, Varrelmann M. Ursachen und auswirkungen des auftretens von “syndrome des basses richesses” in deutschen zuckerrübenanbaugebieten. Sugar Ind. 2020;145:234–44.
Behrmann SC, Witczak N, Lang C, Schieler M, Dettweiler A, Kleinhenz B, et al.. Biology and rearing of an emerging sugar beet pest: The planthopper Pentastiridius leporinus. Insects. 2022. Jul 21;13(7):656. doi: 10.3390/insects13070656 PubMed DOI PMC
Zübert C, Kube M. Application of TaqMan Real-Time PCR for detecting ‘Candidatus Arsenophonus phytopathogenicus’ infection in sugar beet. Pathogens. 2021. Nov;10(11):1466. doi: 10.3390/pathogens10111466 PubMed DOI PMC
Doyle J, Doyle J. Isolation of plant DNA from fresh tissue. Focus. 1990;12:13–5.
Deng S, Hiruki C. Amplification of 16S rRNA genes from culturable and nonculturable mollicutes. J Microbiol Methods. 1991;14(1):53–61.
Schneider B. Phylogenetic classification of plant pathogenic mycoplasma-like organisms or phytoplasma. Molecular and Diagnostic Procedures in Mycoplasmolgy. 1995;1:369–80.
Lee I, Bertaccini A, Vibio M, Gundersen D. Detection of multiple phytoplasmas in perennial fruit trees with decline symptoms in Italy. Phytopathology. 1995;85(6):728–35.
Mitrović J, Siewert C, Duduk B, Hecht J, Mölling K, Broecker F, et al.. Vol. 24,Generation and analysis of draft sequences of ’stolbur’ phytoplasma from multiple displacement amplification templates. J Mol Microbiol Biotechnol. 2014;24(1):1–11. doi: 10.1159/000353904 PubMed DOI
Schneider B, Gibb KS. Sequence and RFLP analysis of the elongation factor Tu gene used in differentiation and classification of phytoplasmas. Microbiology. 1997;143(10):3381–9. doi: 10.1099/00221287-143-10-3381 PubMed DOI
Kosovac A. The Influence of host-plant use on cryptic differentiation of vector Hyalesthes obsoletus Signoret, 1865 (Hemiptera: Cixiidae) and on epidemiological transmission routes of ‘Candidatus Phytoplasma solani’. University of Belgrade, Serbia; 2018.
Fabre A, Danet JL, Foissac X. The stolbur phytoplasma antigenic membrane protein gene stamp is submitted to diversifying positive selection. Gene. 2011. Feb;472(1–2):37–41. doi: 10.1016/j.gene.2010.10.012 PubMed DOI
Namba S Detection and differentiation of plant-pathogenic mycoplasmalike organisms using polymerase chain reaction. Phytopathology. 1993;83(9):786.
Gibb K, Padovan AC, Mogen BD. Studies on sweet potato little-leaf phytoplasma detected in sweet potato and other plant species growing in Northern Australia. Phytopathology. 1995;85(2):169.
Lee IM, Hammond RW, Davis RE, Gundersen DE. Universal amplification and analysis of pathogen 16S rDNA for classification and identification of mycoplasmalike organisms. Phytopathology. 1993;83(8):834–42.
Staden R, Beal KF, Bonfield JK. The Staden package. Methods Mol Biol. 2000;132:115–30. PubMed
Aryan A, Brader G, Mörtel J, Pastar M, Riedle-Bauer M. An abundant ‘Candidatus Phytoplasma solani’ tuf b strain is associated with grapevine, stinging nettle and Hyalesthes obsoletus. Eur J Plant Pathol. 2014. Oct 1;140(2):213–27. doi: 10.1007/s10658-014-0455-0 PubMed DOI PMC
Langer M, Maixner M. Molecular characterisation of grapevine yellows associated phytoplasmas of the stolbur-group based on RFLP-analysis of non-ribosomal DNA. VITIS—Journal of Grapevine Research. 2004;43(4):191–9.
Jamshidi E, Murolo S, Salehi M, Romanazzi G. Sequence analysis of new Tuf molecular types of ‘Candidatus Phytoplasma solani’ in Iranian Vineyards. Pathogens. 2020. Jun;9(6):508. doi: 10.3390/pathogens9060508 PubMed DOI PMC
Balakishiyeva G, Bayramova J, Mammadov A, Salar P, Danet JL, Ember I, et al.. Important genetic diversity of ‘Candidatus Phytoplasma solani’ related strains associated with bois noir grapevine yellows and planthoppers in Azerbaijan. Eur J Plant Pathol. 2018;151:937–46.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018. Jun 1;35(6):1547–9. doi: 10.1093/molbev/msy096 PubMed DOI PMC
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997. Dec 1;25(24):4876–82. doi: 10.1093/nar/25.24.4876 PubMed DOI PMC
Kosovac A, Ćurčić Ž, Stepanović J, Rekanović E, Duduk B. Epidemiological role of novel and already known ‘Ca. P. solani’ cixiid vectors in rubbery taproot disease of sugar beet in Serbia. Sci Rep. 2023;13(1):1433. doi: 10.1038/s41598-023-28562-8 PubMed DOI PMC
Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Bioinformatics. 1992;8(3):275–82. doi: 10.1093/bioinformatics/8.3.275 PubMed DOI
Lee IM, Zhao Y, Bottner KD. SecY gene sequence analysis for finer differentiation of diversestrains in the aster yellows phytoplasma group. Mol Cell Probes. 2006;20(2):87–91. doi: 10.1016/j.mcp.2005.10.001 PubMed DOI
Martini M, Lee IM, Bottner KD, Zhao Y, Botti S, Bertaccini A, et al.. Ribosomal protein gene-based phylogeny for finer differentiation and classification of phytoplasmas. Int J Syst Evol Microbiol. 2007;57(9):2037–51. doi: 10.1099/ijs.0.65013-0 PubMed DOI
Zreik L, Bove JM, Garnier M. Phylogenetic characterization of the bacterium-like organism associated with marginal chlorosis of strawberry and proposition of a Candidatus taxon for the organism, ‘Candidatus Phlomobacter fragariae’. Int J Syst Bacteriol. 1998. Jan 1;48(1):257–61. PubMed
Sémétey O, Bressan A, Gatineau F, Boudon‐Padieu E. Development of a specific assay using RISA for detection of the bacterial agent of ‘basses richesses’ syndrome of sugar beet and confirmation of a Pentastiridius sp. (Fulgoromopha, Cixiidae) as the economic vector. Plant Pathol. 2007;56(5):797–804.
Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 1991;173(2):697–703. doi: 10.1128/jb.173.2.697-703.1991 PubMed DOI PMC
Sarr MP, Groenewald JZ, Crous PW. Genetic diversity in Macrophomina phaseolina, the causal agent of charcoal rot. Phytopathol Mediterr. 2014;53(2):250.
Day JP, Shattock RC. Aggressiveness and other factors relating to displacement of populations of Phytophthora infestans in England and Wales. Eur J Plant Pathol. 1997. May 1;103(4):379–91.
Santos KM, Lima GS, Barros AP, Machado AR, Souza-Motta CM, Correia KC, et al.. Novel specific primers for rapid identification of Macrophomina species. Eur J Plant Pathol. 2020;156:1213–8.
Jacobs K, Bergdahl DR, Wingfield MJ, Halik S, Seifert KA, Bright DE, et al.. Leptographium wingfieldii introduced into North America and found associated with exotic Tomicus piniperda and native bark beetles. Mycol Res. 2004;108(4):411–8. doi: 10.1017/s0953756204009748 PubMed DOI
Carbone I, Kohn LM. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia. 1999;91(3):553–6.
White T, Bruns T, Lee S, Taylor W. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: A Guide to Methods and Applications. New York: Academic Press, Inc.; 1990. p. 315–22.
Glass NL, Donaldson GC. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol. 1995;61(4):1323–30. doi: 10.1128/aem.61.4.1323-1330.1995 PubMed DOI PMC
O’Donnell K, Cigelnik E. Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol. 1997;7(1):103–16. doi: 10.1006/mpev.1996.0376 PubMed DOI
Hasegawa M, Kishino H, aki Yano T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 1985;22:160–74. PubMed
Quaglino F, Passera A, Faccincani M, Moussa A, Pozzebon A, Sanna F, et al.. Molecular and spatial analyses reveal new insights on bois noir epidemiology in Franciacorta vineyards. Ann Appl Biol. 2021;179(2):151–68.
Pierro R, Panattoni A, Passera A, Materazzi A, Luvisi A, Loni A, et al.. Proposal of a new bois noir epidemiological pattern related to ‘Candidatus Phytoplasma solani’ strains characterized by a possible moderate virulence in Tuscany. Pathogens. 2020. Apr;9(4):268. doi: 10.3390/pathogens9040268 PubMed DOI PMC
Bressan A, Terlizzi F, Credi R. Independent origins of vectored plant pathogenic bacteria from arthropod-associated Arsenophonus endosymbionts. Microb Ecol. 2012. Apr 1;63(3):628–38. doi: 10.1007/s00248-011-9933-5 PubMed DOI
Racovita A. Noi cercetari privind gomoza sfeclei de zahar. Extras din Lucră rile Institutului de cercetări alimentare. 1959;3:269–96.
Zwolińska A, Krawczyk K, Klejdysz T, Pospieszny H. First report of ‘Candidatus Phytoplasma asteris’ associated with oilseed rape phyllody in Poland. Plant Dis. 2011. Nov;95(11):1475–1475. doi: 10.1094/PDIS-03-11-0177 PubMed DOI
Zwolińska A, Borodynko‐Filas N. Intra and extragenomic variation between 16S rRNA genes found in 16SrI‐B‐related phytopathogenic phytoplasma strains. Ann Appl Biol. 2021;179(3):368–81.
Duduk B, Calari A, Paltrinieri S, Duduk N, Bertaccini A. Multigene analysis for differentiation of aster yellows phytoplasmas infecting carrots in Serbia. Ann Appl Biol. 2009;154(2):219–29.
Zwolińska A, Krawczyk K, Borodynko-Filas N, Pospieszny H. Non-crop sources of rapeseed phyllody phytoplasma (‘Candidatus Phytoplasma asteris’: 16SrI-B and 16SrI-(B/L)L), and closely related strains. Crop Prot. 2019. May 1;119:59–68.
Villaréal LM, Lannou C, de Vallavieille-Pope C, Neema C. Genetic variability in Puccinia striiformis f. sp. tritici populations sampled on a local scale during natural epidemics. Appl Environ Microbiol. 2002;68(12):6138. doi: 10.1128/AEM.68.12.6138-6145.2002 PubMed DOI PMC
Rousseau E, Bonneault M, Fabre F, Moury B, Mailleret L, Grognard F. Virus epidemics, plant-controlled population bottlenecks and the durability of plant resistance. Philos Trans R Soc Lond B Biol Sci. 2019. Jun 24;374(1775):20180263. doi: 10.1098/rstb.2018.0263 PubMed DOI PMC
Terlizzi F, Babini AR, Lanzoni C, Pisi A, Credi R, Foissac X, et al.. First report of a γ 3-Proteobacterium associated with diseased strawberries in Italy. Plant Dis. 2007;91(12):1688–1688. PubMed
Nováková E, Hypša V, Moran NA. Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol. 2009. Jul 20;9(1):143. doi: 10.1186/1471-2180-9-143 PubMed DOI PMC
Salar P, Sémétey O, Danet JL, Boudon-Padieu E, Foissac X. ‘Candidatus Phlomobacter fragariae’ and the proteobacterium associated with the low sugar content syndrome of sugar beet are related to bacteria of the arsenophonus clade detected in hemipteran insects. Eur J Plant Pathol. 2010. Jan 1;126(1):123–7.
Behrmann SC, Rinklef A, Lang C, Vilcinskas A, Lee KZ. Potato (Solanum tuberosum) as a new host for Pentastiridius leporinus (Hemiptera: Cixiidae) and ‘Candidatus Arsenophonus phytopathogenicus‘. Insects. 2023. Mar;14(3):281. PubMed PMC
Stojšin VB, Marić AA, Jasnić SM, Bagi FF, Marinković BJ. Root rot of sugarbeet in the Vojvodina Province. Zbornik matice srpske za prirodne nauke. 2006;(110):65–74.