Clonality, spatial structure, and pathogenic variation in Fusarium fujikuroi from rain-fed rice in southern Laos
Autoři:
Barbara Scherm aff001; Virgilio Balmas aff001; Alessandro Infantino aff002; Maria Aragona aff002; Maria Teresa Valente aff002; Francesca Desiderio aff003; Angela Marcello aff001; Sengphet Phanthavong aff004; Lester W. Burgess aff005; Domenico Rau aff006
Působiště autorů:
Dipartimento di Agraria, Sezione di Patologia ed Entomologia, Università degli Studi di Sassari, Sassari, Italy
aff001; Council for Agricultural Research and Economics (CREA), Research Centre for Plant Protection and Certification, Rome, Italy
aff002; Council for Agricultural Research and Economics, Research Centre for Genomics and Bioinformatics, Fiorenzuola d’Arda (PC), Italy
aff003; Provincial Agriculture and Forestry, Thaluang Village, Pakse, Champasak, Lao PDR
aff004; Sydney Insitute of Agriculture, Faculty of Science, University of Sydney, New South Wales, Australia
aff005; Dipartimento di Agraria, Sezione di Patologia ed Entomologia, Università degli Studi di Sassari, Sassari, Italy
aff006
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0226556
Souhrn
Bakanae disease, caused by the fungal phytopathogen Fusarium fujikuroi, can be detected in most rice (Oryza sativa L.) growing areas worldwide. In this study, we investigated the population structure of this fungus in southern Lao PDR, a country located near the geographic origin of rice domestication. Microsatellites (SSRs) and mating type (MAT) analyses, pathogenicity and fungicide sensitivity tests were integrated in the study. The first key finding is that the population genetic structure of F. fujikuroi in Lao PDR is consistent with high clonal reproduction. Indeed, (i) “true” clones were identified; (ii) within populations, MAT types were frequently skewed from 1:1 ratio, (iii) linkage disequilibrium (among SSRs as also among SSRs and MAT) was present, and (iv) gene-flow between opposite MAT types within the same population is restricted. The presence of genetic divergence among areas and populations and the occurrence of positive spatial autocorrelation of genetic variation, indicate that migration is restricted, and that genetic drift plays an important role in the evolution of this fungus. Two main well-defined groups of isolates were detected (FST = 0.213) that display a non-random spatial distribution. They differ in the ability to induce seedlings death but not seedlings elongation (the typical Bakanae symptom) suggesting that the pathogen’s ability to induce the two symptoms is under different genetic control. Finally, we compared two agroecosystems with contrasting characteristics: low-input and traditional (Lao PDR) vs high-input and modern (Italy). We found differences in the level of population structuring and of spatial autocorrelation. This suggests that the evolutionary potential of the fungus not only depends on its intrinsic characteristics, but is strongly influenced by other external factors, most likely by the dynamics of infested seed exchange. Thus, quarantine and chemical treatments are a way to reduce population connectivity and hence the evolutionary potential of this pathogen.
Klíčová slova:
Haplotypes – Rice – Fungal genetics – Population genetics – Fungal structure – Italy – Fusarium – Laos
Zdroje
1. Ou SH. Rice Diseases. 2nd ed. CAB International, Commonwealth Mycological Institute, Kew, UK; 1985.
2. Bashyal BM. Etiology of an emerging disease: Bakanae of rice. Indian Phytopathol. 2018; 71:485–494.
3. Singh R, Kumar P, Laha GS. Present status of Bakanae of rice caused by Fusarium fujikuroi Nirenberg. Indian Phytopathol. 2019;1–11. https://doi.org/10.1007/s42360-019-00125-w
4. Nurul Faziha I, Masratul Hawa M, Nik Mohd Izham MN, Latiffah Z. Fusarium fujikuroi causing fusariosis of pineapple in peninsular Malaysia. Austral. Plant Dis. Notes. 2016;11–21. https://doi.org/10.1007/s13314-016-0206-5.
5. Pedrozo R, Fenoglio JJ, Little CR. First report of seedborne Fusarium fujikuroi and its potential to cause pre- and post-emergent damping-off on Soybean (Glycine max) in the United States. Plant Dis. 2015;99(12):1865–.
6. Gupta AK, Solanki IS, Bashyal BM, Singh Y, Srivastava K. Bakanae of Rice—an Emerging Disease in Asia. J Anim Plant Sci. 2015;25(6):1499–1514.
7. Jiang SB, Lin BR, Shen HF, Yang QY, Zhang JX, Sun DY, et al. First report of Fusarium fujikuroi causing stem wilt on Canna edulis Ker in China. Plant Dis. 2018;102(6):1177–1177.
8. Masratul Hawa M, Faziha IN, Izham MNNM, Latiffah Z. Fusarium fujikuroi associated with stem rot of red-fleshed dragon fruit (Hylocereus polyrhizus) in Malaysia. Ann Appl Biol. 2017;170(3):434–446.
9. Pinaria AG, Liew ECY, Burgess LW. Fusarium species associated with vanilla stem rot in Indonesia. Australas Plant Path. 2010;39(2):176–183.
10. Chang DC, Grant GB, O'Donnell K, Wannemuehler KA, Noble-Wang J, Rao CY, et al. Multistate outbreak of Fusarium keratitis associated with use of a contact lens solution. Jama-J Am Med Assoc. 2006;296(8):953–963.
11. Valente MT, Desiderio F, Infantino A, Vale G, Abbruscato P, Aragona M. Genetic variability of Fusarium fujikuroi populations associated with bakanae of rice in Italy. Plant Pathol. 2017;66(3):469–479.
12. Prasad R, Shivay YS, Kumar D. Current Status, Challenges, and Opportunities in Rice Production. In: Chauhan BS, Jabran K, Mahajan G editors. Rice Production Worldwide. Springer International Publishing AG, Switzerland. 2017. p 1–32
13. Eliste P and. Santos N. Lao people’s democratic republic rice policy study. Washington DC; World Bank. http://documents.worldbank.org/curated/en/2012/01/17783012/lao-peoplesdemocratic-republic-rice-policy-study; 2012.
14. Schiller JM., ed Chanphengxay MBed, Linquist B, and Appa Rao S, editors. Rice in Laos. Los Baños, Philippines: International Rice Research Institute; 2006.
15. Callaway E. The birth of rice. Nature. 2014;514(7524):S58–S59. doi: 10.1038/514s58a 25368889
16. Saleh D, Milazzo J, Adreit H, Fournier E, Tharreau D. South-East Asia is the center of origin, diversity and dispersion of the rice blast fungus, Magnaporthe oryzae. New Phytol. 2014;201(4):1440–1456. doi: 10.1111/nph.12627 24320224
17. Schiller JM, Linquist B, Douangsila K, Inthapanya P,>Douang Boupha B, Inthavong S, et al. Constraints to rice production systems in Laos. In: Fukai S, Basnayake J, editors. Increased lowland rice production in the Mekong Region. Proceedings of an International Workshop, Vientiane, Laos, 30 Oct.-2 Nov. 2000. ACIAR Proceedings No.101. Canberra (Australia): ACIAR. p 3–19; 2001.
18. Douangboupha B, Khamphoukeo K, Inthavong S, Schiller J, and Jahn G. Pests and diseases of the rice production systems of Laos. In: Schiller JM., Chanphengxay MB, Linquist B, and Appa Rao S, editors. Rice in Laos. Los Baños, Philippines, International Rice Research Institute, 2006; pp. 265–281.
19. Infantino A, Balmas V, Scherm B, Orzali L, Ireland KB, Laurence MH, et al. First report of Fusarium fujikuroi in the Lao PDR. Australas Plant Dis. Notes. 2017;12:14. https://doi.org/10.1007/s13314-017-0238-5
20. O'Donnell K, Cigelnik E, Nirenberg HI. Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia. 1998;90(3):465–93.
21. Leslie JF. Gibberella fujikuroi—available populations and variable traits. Can J Bot. 1995;73:S282–S91.
22. Leslie JF, Anderson LL, Bowden RL, Lee YW. Inter- and intra-specific genetic variation in Fusarium. Int J Food Microbiol. 2007;119(1–2):25–32. doi: 10.1016/j.ijfoodmicro.2007.07.059 17854936
23. Leslie J. and Summerell B. The Fusarium laboratory manual. Oxford, UK: Blackwell Publishing Ltd. 2006
24. McDonald BA, Linde C. The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica. 2002;124(2):163–80.
25. Carter LLA, Leslie JF, Webster RK. Population structure of Fusarium fujikuroi from California rice and water grass. Phytopathology. 2008;98(9):992–8. doi: 10.1094/PHYTO-98-9-0992 18943737
26. Cumagun CR, Gonzalez-Jaen M, Aguilar KI, Varona AC, Marin P. Phylogenetic analysis, fumonisin production, and genetic variability of Fusarium fujikuroi strains isolated from rice in the Philippines. Phytopathology. 2012;102(7):27–.
27. Cruz A, Marin P, Gonzalez-Jaen MT, Aguilar KGI, Cumagun CJR. Phylogenetic analysis, fumonisin production and pathogenicity of Fusarium fujikuroi strains isolated from rice in the Philippines. J Sci Food Agr. 2013;93(12):3032–9.
28. Chen YC, Lai MH, Wu CY, Lin TC, Cheng AH, Yang CC, et al. The genetic structure, virulence, and fungicide sensitivity of Fusarium fujikuroi in Taiwan. Phytopathology. 2016;106(6):624–35. doi: 10.1094/PHYTO-11-15-0285-R 26882848
29. Benali S, Mohamed B, Eddine HJ, Neema C. Advances of molecular markers application in plant pathology research. Eur J Sci Res. 2011;50: 110–123.
30. Capote N, Pastrana AM, Aguado A, Sanchez-Torres P. Molecular tools for detection of plant pathogenic fungi and fungicide resistance. In: Cumagun CJ, editor. Plant pathology. Rijeka: InTech, Croatia; 2012; pp. 151–202.
31. Burgess LW, Summerell BA, Bullock S, Gott KP and Backhouse D. Laboratory manual for Fusarium research. Sydney: University of Sydney; 1994.
32. Nelson PE, Toussoun TA and Marasas WFO. Fusarium species: An illustrated manual for identification. Pennsylvania, USA: Pennsylvania State University Press; 1983.
33. Aljanabi SM, Martinez I. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res. 1997;25(22):4692–4693. doi: 10.1093/nar/25.22.4692 9358185
34. Amatulli MT, Spadaro D, Gullino ML, Garibaldi A. Conventional and real-time PCR for the identification of Fusarium fujikuroi and Fusarium proliferatum from diseased rice tissues and seeds. Eur J Plant Pathol. 2012;134(2):401–408.
35. Martin SH, Wingfield BD, Wingfield MJ, Steenkamp ET. Structure and evolution of the Fusarium mating type locus: new insights from the Gibberella fujikuroi complex. Fungal Genet Biol. 2011;48(7):731–740. doi: 10.1016/j.fgb.2011.03.005 21453780
36. Schuelke M. An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol. 2000;18(2):233–234. doi: 10.1038/72708 10657137
37. Zainudin N, Razak AA, Salleh B,. Bakanae disease of rice in Malaysia and Indonesia: etiology of the causal agent based on morphological, physiological and pathogenicity characteristics. J Pl Prot Res. 2008; 48: 475–485.
38. McKinney HH, Influence of soil temperature and moisture on infection of wheat seedlings by Helminthosporium sativum. J Agric Res. 1923; 26:195–217.
39. Nei M. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics. 1978;89(3):583–590. 17248844
40. Excoffier L, Lischer HE. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10(3):564–567. doi: 10.1111/j.1755-0998.2010.02847.x 21565059
41. Wright S. The genetical structure of populations. Ann Eugen. 1951;15(4):323–354 doi: 10.1111/j.1469-1809.1949.tb02451.x 24540312
42. Excoffier L, Smouse PE, Quattro JM. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 1992;131(2):479–491. 1644282
43. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155(2):945–959. 10835412
44. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14(8):2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x 15969739
45. Earl DA, Von Holdt BM. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 2012;4(2):359–361.
46. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol. 2018;35(6):1547–1549. doi: 10.1093/molbev/msy096 29722887
47. Beugin MP, Gayet T, Pontier D, Devillard S, Jombart T. A fast likelihood solution to the genetic clustering problem. Methods Ecol Evol. 2018;9(4):1006–1016. doi: 10.1111/2041-210X.12968 29938015
48. Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24(11):1403–1405. doi: 10.1093/bioinformatics/btn129 18397895
49. Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 2010;11. doi: 10.1186/1471-2156-11-11
50. Mantel N. The detection of disease clustering and a generalized regression approach. Cancer Res. 1967;27(2):209–220. 6018555
51. Jombart T, Devillard S, Dufour AB, Pontier D. Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity. 2008;101(1):92–103. doi: 10.1038/hdy.2008.34 18446182
52. Moran PAP. The interpretation of statistical maps. J R Stat Soc B. 1948; 37(2):243–251.
53. Jombart T and Collins C. A tutorial for discriminant analysis of principal components (DAPC) using adegenet 2.0. 0. London: Imperial College London, MRC Centre for Outbreak Analysis and Modelling; 2015.
54. Peakall ROD and Smouse PE. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecol notes. 2006; 6(1): 288–295.
55. Banks SC, Peakall R. Genetic spatial autocorrelation can readily detect sex-biased dispersal. Mol Ecol. 2012;21(9):2092–2105. doi: 10.1111/j.1365-294X.2012.05485.x 22335562
56. Smouse PE, Peakall R, Gonzales E. A heterogeneity test for fine-scale genetic structure. Mol Ecol. 2008;17(14):3389–3400. doi: 10.1111/j.1365-294x.2008.03839.x 18677808
57. Agapow PM, Burt A. Indices of multilocus linkage disequilibrium. Mol Ecol Notes. 2001;1(1–2):101–102.
58. Smith JM, Smith NH, Orourke M, Spratt BG. How clonal are bacteria? P Natl Acad Sci USA. 1993;90(10):4384–4388.
59. Chen RS, McDonald BA. Sexual reproduction plays a major role in the genetic structure of populations of the fungus Mycosphaerella graminicola. Genetics. 1996;142(4):1119–1127. 8846892
60. Rau D, Brown AHD, Brubaker CL, Attene G, Balmas V, Saba E, et al. Population genetic structure of Pyrenophora teres Drechs. the causal agent of net blotch in Sardinian landraces of barley (Hordeum vulgare L.). Theor Appl Genet. 2003;106(5):947–959. doi: 10.1007/s00122-002-1173-0 12647071
61. Tibayrenc M, Kjellberg F, Ayala FJ. A clonal theory of parasitic protozoa—the population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas, and Trypanosoma and their medical and taxonomical consequences. P Natl Acad Sci USA. 1990;87(7):2414–2418.
62. Arnaud-Haond S, Duarte CM, Alberto F, Serrao EA. Standardizing methods to address clonality in population studies. Mol Ecol. 2007;16(24):5115–5139. doi: 10.1111/j.1365-294X.2007.03535.x 17944846
63. Stenberg P, Lundmark M, Saura A. MLGsim: a program for detecting clones using a simulation approach. Mol Ecol Notes. 2003;3(2):329–331.
64. Linde CC, Zala M, Ceccarelli S, McDonald BA. Further evidence for sexual reproduction in Rhynchosporium secalis based on distribution and frequency of mating-type alleles. Fungal Genet Biol. 2003;40(2):115–125. doi: 10.1016/s1087-1845(03)00110-5 14516764
65. Rau D, Maier FJ, Papa R, Brown AHD, Balmas V, Saba E, et al. Isolation and characterization of the mating-type locus of the barley pathogen Pyrenophora teres and frequencies of mating-type idiomorphs within and among fungal populations collected from barley landraces. Genome. 2005;48(5):855–869. doi: 10.1139/g05-046 16391692
66. Lewontin RC., and Felsenstein J. The robustness of homogeneity tests in 2 × N tables. Biometrics 1965; 21:19–33.
67. Sokal RR. and Rohlf FJ. Biometry: The Principles and Practice of Statistics in Biological Research. 3rd Edition, W.H. Freeman and Co., New York; 1995
68. Rau D, Attene G, Brown AHD, Nanni L, Maier FJ, Balmas V, et al. Phylogeny and evolution of mating-type genes from Pyrenophora teres, the causal agent of barley "net blotch" disease. Curr Genet. 2007;51(6):377–392. doi: 10.1007/s00294-007-0126-1 17426975
69. Rau D, Rodriguez M, Murgia ML, Balmas V, Bitocchi E, Bellucci E, et al. Co-evolution in a landrace metapopulation: two closely related pathogens interacting with the same host can lead to different adaptive outcomes. Sci Rep. 2015;5, 12834. doi: 10.1038/srep12834 26248796
70. Richman A. Evolution of balanced genetic polymorphism. Mol Ecol. 2000;9(12):1953–63. doi: 10.1046/j.1365-294x.2000.01125.x 11123608
71. Douhan GW, Murray TD, Dyer PS. Species and mating-type distribution of Tapesia yallundae and T.-acuformis and occurrence of apothecia in the US Pacific Northwest. Phytopathology. 2002;92(7):703–709. doi: 10.1094/PHYTO.2002.92.7.703 18943265
72. Brasier CM, Webber JF. Positive correlations between in-vitro growth rate and pathogenesis in Ophiostoma-ulmi. Plant Pathol. 1987;36(4):462–466.
73. Kaltz O, Shykoff JA. Selfing versus outcrossing propensity of the fungal pathogen Microbotryum violaceum across Silene latifolia host plants. J Evolution Biol. 1999;12(2):340–349.
74. Halama P. Mating relationships between isolates of Phaeosphaeria nodorum, (anamorph Stagonospora nodorum) from geographical locations. Eur J Plant Pathol. 2002;108(6):593–596.
75. Meng JW, He DC, Zhu W, Yang LN, Wu EJ, Xie JH, et al. Human-mediated gene flow contributes to metapopulation genetic structure of the pathogenic fungus Alternaria alternata from potato. Front Plant Sci. 2018;9:198. doi: 10.3389/fpls.2018.00198 29497439
76. Niehaus EM, Kim HK, Munsterkotter M, Janevska S, Arndt B, Kalinina SA, et al. Comparative genomics of geographically distant Fusarium fujikuroi isolates revealed two distinct pathotypes correlating with secondary metabolite profiles. Plos Pathog. 2017;13(10):e1006670. doi: 10.1371/journal.ppat.1006670 29073267
77. Choi HW, Hong SK, Lee YK, Kim WG, Chun S. Taxonomy of Fusarium fujikuroi species complex associated with Bakanae on rice in Korea. Australas Plant Path. 2018;47(1):23–34.
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