ATLANTIC FOREST MEDICINAL PLANT Aristolochia triangularis Cham (ARISTOLOCHIACEAE) AS SOURCE OF FUNGAL ENDOPHYTES CAPABLE OF CONTROLLING STRAWBERRY DISEASES

ANDRESSA KATISKI DA COSTA STUART¹*, RODRIGO MAKOWIECKY STUART², IDA CHAPAVAL PIMENTEL^3
1Department of Basic Pathology, Sector of Biological Sciences, Federal University of Paraná, Curitiba, Paraná, Brazil
²Department of Basic Pathology, Sector of Biological Sciences, Federal University of Paraná, Curitiba, Paraná, Brazil
³Department of Basic Pathology, Sector of Biological Sciences, Federal University of Paraná, Curitiba, Paraná, Brazil
* Corresponding Author : andressa.katiski@gmail.com

Received : 19-07-2018     Accepted : 23-08-2018     Published : 30-08-2018
Volume : 10     Issue : 8       Pages : 1325 - 1337
Int J Microbiol Res 10.8 (2018):1325-1337

Keywords : Biocontrol, Endophytes, Biodiversity, Polyketides, Bioactive compounds
Academic Editor : Manoj Kumar Solanki, Mariana Porsani
Conflict of Interest : None declared
Acknowledgements/Funding : We are grateful to Biochemical sector of the Federal University of Paraná for use its facilities. This work was financed by Coordenação de Aperfeiçoamento do Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)
Author Contribution : All author equally contributed

Atlantic Forest is one of the richest biomes of the world. Among their plants, Aristolochia triangularis stands out by its uses in Brazilian popular medicine. Endophytic fungi live inside plants producing several bioactive metabolites. They may, therefore, be used in biological control. Strawberry culture is one of the most important cultures worldwide. Its main phytopathogens are Botrytis cinerea and Rhizopus stolonifer. Biological control, are being used to control this kind of pathogens. In this work, a total of 263 endophytes were isolated from A. triangularis. They were submitted to ARDRA assay, resulting in 26 different haplotypes, representing 9 families and 13 different genera. Dual culture test showed 7 isolates capable to promote biological control of these pathogens in vitro. A total of 66 isolates showed presence of Polyketide synthase (PKS) I, a gene linked to bioactive metabolites production. PKS presence in the isolates, demonstrate their ability to produce bioactive compounds.

1. MMA – Ministéro do Meio Ambiente, Brazilian Government (2017) [http://www.mma.gov.br/biomas/mata-atlantica]]
2. Correa C.F. and Biasi, L.A. (2003) Revista Brasileira de Agrociências 9(3), 233,235.
3. Souza G.C., Haas A.P.S., Von Poser G.L., Schapoval E.E.S. and Elisabetsky E. (2004) Journal of Ethnopharmacology 90, 135,143.
4. Alvin A., Miller K.I. and Neilan B.A. (2014) Microbiological Research 169, 483,495.
5. Schulz, B.J.E. and Boyle, C.J.C. (2006) What are endophytes? In Microbial Root Endophytes ed. Schulz, B.J.E, Boyle, C.J.C, Sieber, T.N. Verlag, Berlin.
6. Abrahão M.R.E., Molina G. and Pastore G.M. (2013) Food Research International 52, 367,372.
7. Tan R.X. and Zou W.X. (2001) Natural Product Reports 18, 448,459.
8. Miller K.I., Qing C., Sze D.M.Y. and Neilan B.A. (2012a) Plos One 7(5), 1,12.
9. Strobel G., Daisy B., Castillo U. and Harper J. (2004) Journal of Natural Products 67, 257,268.
10. Bale J.S., Lenteren J.C. and Bigler F. (2008) Philosophical Transactions of the Royal Society B 363, 761,776.
11. Camargo L.K.P., Resende J.T.V., Galvão A.G., Camargo C.K. and Baier J.E. (2010) Ambiência 6(2), 281,288.
12. Morales R.G.F., Faria M.V., Resende J.T.V., Rissini A.L.L., Carminatti R. and Faria C.M.D.R. (2012) Ambiência 8(1), 23,33.
13. FAOSTAT – Food and Agriculture Organization of the United States (2018). [http://www.fao.org/faostat/en/#rankings/countries_by_commodity]
14. Romanazz] G., Feliziani E., Santini M. and Landi L. (2013) Postharvest Biology and Technology 75, 24,27.
15. Jia N., Xie Y., Zhang H., Liu H., Feng J., Zhu L. and Zhou X. (2012) Advanced Materials Research 554, 1547,1552.
16. Ilhan K. and Karabulut O.A. (2013) Biological Control 58, 457,470.
17. Matyjaszczyk E. (2015) Pest Management Science 71(9), 1201,1206.
18. Amnuaykanjanasin A., Punya J., Paungmoung P., Rungrod A., Tachaleat A., Pongpattanakitshote S., Cheevadhanarak S. and Tanticharoen M. (2005) FEMS Microbiology Letters 251, 125,136.
19. Wang G., Liu Z., Lin R., Li E., Mao Z., Ling J., Yang Y., Yin W.B. and Xie B. (2016a) Plos Pathogens 12(7), p. e1005685.
20. Campbell C.D. and Vederas J.C. (2010) Biopolymers 93(9), 755,763.
21. Wang W.X., Kusari S., Laatsch H., Golz C., Kusari P., Strohmann C., Kayser O. and Spiteller M. (2016b) Journal of Natural Products 79,704,710.
22. Yao L., Tan C., Song J., Yang Q., Yu L., Li X. (2016) Brazilian Journal of microbiology 47, 468,479.
23. Atanasova L., Knox B.P., Kubicek C.P., Druzhinina I.S. and Baker S.E. (2013) Eukaryotic Cell 12(11),1499,1508.
24. Evans B.S., Robinson S.J. and Kelleher N.L. (2011) Fungal Genetics and Biology 48, 49,61.
25. Miller K.I., Qing C., Sze D.M.Y., Roufogalis B.D. and Neilan B.A. (2012b) Microbial Ecology 64(2), 431,449.
26. Kleiner A.A.P., Ferreira A., Lima A.O.S., Andreote F.D., Andreote F.D., Pimentel I.C., Azevedo J.L., Marcon J., Sobral J.K, Quecine M.C., Martins M.K., Lacava P.T., Rosseto P.B., Stuart R.M. and Araujo W.L. (2010) Guia prático, Isolamento e Caracterização de Microrganismos Endofíticos. Calo, Piracicaba-SP.
27. Vicente V.A., Freitas F., Kleiner A.A.P., Angelis D.A.S. and Telles F.Q. (2001) Revista da Sociedade Brasileira de Medicina Tropical 4(1), 34.
28. White T.J., Bruns T., Lee S. and Taylor J.W. (1990) PCR protocols, a guide to methods and applications ed. Innis M.A., Gelfand D.H., Sninsky J.J., White T.J. Academic Press, San Diego.
29. Vaneechoutte M., Beenhouwer H., Claeys G., Verschraegen G., De Rouck A., Paepe N., Elaichouni A. and Portaels F. (1993) Journal of Clinical Microbiology 31(8), 2061,2065.
30. Camatti-Sartori V., Silva-Ribeiro R.T., Valdebenito-Sanhueza R.M., Pagnocca F.C., Echeverrigaray S. and Azevedo J.L. (2005) Journal of Basic Microbiology 45(5), 397,402.
31. Bongiorno V.A., Rhoden S.A., Garcia A., Polonio J.C., Azevedo J.L., Pereira J.O. and Pamphile J.A. (2016) Annals of Microbiology 68, 855,865.
32. Campanile G., Ruscelli A. and Luisi N. (2007) European Journal of Plant Pathology 117, 237,246.
33. Bingle L.E.H., Simpson T.J. and Lazarus C.M. (1999) Fungal Genetics and Biology 26, 209,223.
34. Glynou K., Ali T., Buch A.K., Kia S.H., Ploch S., Xia X., Çelik A., Thines M. and Maciá-Vicente J.G. (2015) Environmental MIcrobiology 18, 2418,2434.
35. Wearn J.A., Sutton B.C., Morley N.J. and Gange A.C. (2012) Journal of Ecology 5, 1085,1092.
36. Wang Y. and Guo L.D. (2007) Canadian Journal of Botany 85, 911,917.
37. Cannon P.F. and Simmons C.M. (2002) Mycology 94(2), 210,220.
38. Giauque H. and Hawkes C.V. (2016) Fungal Ecology 20,108,114.
39. Stuart R.M., Romão A.S., Kleiner A.A.P., Azevedo J.L. and Araujo W.L. (2010) Archives Microbiology 192, 307,313.
40. Tabarelli M., Aguiar A.V., Ribeiro M.C., Metzger J.P. and Peres C.A. (2010) Biological Conservation 143, 2328,2340.
41. Venkatachalam S., Ranjan K., Prasanna R., Ramakrishnan B., Trapa S. and Kanchan A. (2016) Plant Biology 18, 627,637.
42. Sangeetha B.G., Jayaprakas C.A., Siji J.V., Rajitha M., Shyni B. and Mohandas C. (2016) 3 Biotech 6, 32.
43. Göre M.E. and Bucak C. (2007) Forest Pathology 37, 281,288.
44. García E., Alonso A., Platas G. and Sacristán S. (2013) Fungal Diversity 60,71,89.
45. Pimentel I.C., Juarez G., Poitevin C.G., Stuart A.K.C. and Azevedo J.L. (2016) Asian Journal of Microbiology Biotechnology and Environmental Science 18(1), 47,53.
46. Saucedo-Garcia A., Anaya A.L., Espinosa-García F.J. and González M.C. (2014) Plos One 9(6), pe98454.
47. Lu H., Zou W.X., Meng J.C., Hu J., Tan R.X. (2000) Plant Science 151(1), 67,73.
48. Shankar S.S., Ahmad A., Pasricha R. and Sastry M. (2003) Journal of Materials Chemistry 13, 1822,1826.
49. Gangadevi V. and Muthumary J. (2008) Mycologia Balcanica 5, 1,4.
50. Monggoot S., Popluechai S., Gentekaki E. and Pripideveech P. (2017) Microbiology Ecology 74(1), 54,61.
51. Hiruma K., Gerlach N., Sacristán S., Nakano R.T., Hacquard S., Kracher, B., Neumann U., Ramirez D., Bucher M.M., O’Connell R.J.M. and Schulze-Lefert P. (2016) Cell 165(2), 464,474.
52. Zou W.X., Meng J.C., Lu H., Chen G.X., Shi G.X., Zhang T.Y., Tan R.X. (2000) Journal of Natural Products 63, 1529,1530.
53. Vu T., Hauschild R. and Sikora R.A. (2006) Nematology 8(6), 847,852.
54. Shen W.Y., Bai R., Wang A.R., He J.Y., Wang H., Zhang Y., Zhao X.F. and Dong J.Y. (2016) Natural Products Research 30(19), 2173,2182
55. Shweta S., Zuehlke S., Ramesha B.T., Priti V., Kumar P.M., Ravikanth G., Spiteller M., Vasudeva R. and Shaanker R.U. (2010) Phytochemistry 71, 117,122.
56. Kour A., Shawl A.S., Rehman S., Sultan P., Qazi P.H., Suden P., Khajuria R.K. and Verma V. (2008) World Journal of Microbiology and biotechnology 24, 1115,1121.
57. Alvin A., Kalaitzis J.A., Sasia B. and Neilan B.A. (2016) Journal of Applied Microbiology 120, 1229,1239.
58. Bayman P. and Otero J.T. (2006) Microbial endophytes of orchid roots. In, Microbial root endophytes ed. Schulz B., Boyle C., SieberT. pp.153,173. New York, Springer.
59. Yuan Z., Chen Y. and Yang Y. (2009) World Journal of Microbiology and Biotechnology 25, 295,303.
60. Oliveira S.F., Bocayuva M.F., Veloso T.G.R., Bazzolli D.M.S., Silva C.C., Pereira O.L. and Kasuya M.C.M. (2014) Mycorrhiza 24, 55,64.
61. Santos I.P., Bezerra J.D.P., Souza-Motta C.M., Cavalcanti M.S. and Lima V.L.M. (2015) African Journal of Microbiology Research 9(18), 1227,1235.
62. Costa L.A. and Gusmão L.F.P. (2017) Journal of Forest Research 28(1), 163,172.
63. Souza C.N. (2010) Diversidade de fungos do solo da mata atlântica. Dissertation, Federal University of Lavras.
64. Reino J.L., Guerrero R.F., Hernández-Galán R. and Collado I.G. (2008) Phytochemistry Reviews 7, 89,123.
65. Saravanakumar K., Yu C., Dou K., Wang M., Li Y. and Chen J. (2016) Biological Control 94, 37,46.
66. Wicklow D., Rogers K.D., Dowd P.F. and Gloer J.B. (2011) Fungal Biology 115,133,142.
67. Horn W.S., Simmonds M.S.J., Schwartz R.E. and Braney W.M. (1995) Tetrahedron 51(14), 3969,3978.
68. Fu J., Zhou Y., Li H.F., Ye Y.H. and Gou J.H. (2011) African Journal of Microbioogyl Research 5(10), 1231,1236.
69. Qadri M., Johri S., Shah B.A., Khajuria A., Sidiq T., Lattoo S.K., Abdin M.Z. and Hassan S.R.U. (2013) Springer Plus 2(1), 8.
70. Banhos E.F., Souza A.Q.L., Andrade J.C., Souza A.D.L., Koolen H.H.F. and Albuquerque P.M. (2014) Brazilian Journal of Microbiology 45(1), 153,161.
71. Toghueo R.M.K., Eke P., Zabalgogeazcoa Í., Aldana B.R.V., Nana L.W.,


72. Boyom F.F. (2016) Biological Control 96, 8,20.
73. Sumida C.H., Daniel J.F.S., Araujod A.P.C.S., Peitl D.C., Abreu L.M., Dekker R.F.H., Canteri M.G. (2018) Biocontrol Science and Technology 28(2), 142,156.
74. Verma M., Brar S.K., Tyagi R.D., Surampalli R.Y., Valéro J.R. (2007) Biochemical Engeneering Journal 37(1), 1,20.
75. Chapla V.M., Zeraik M.L., Leptokarydis I.H., Silva G.H., Bolzani V.S., Young M.C.M. (2014) Molecules 19, 19243,19252.
76. Abdou R., Scherlach K., Dahse H.M., Sattler I., Hertweck C. (2010) Phytochemistry 71, 110,116.
77. Kroken S., Glass N.L., Taylor J.W., Yoder O.C. and Turgeon B.G. (2003) PNAS 100(26), 15670,15675.
78. Gaffor I., Brown D.W., Plattner R., Proctor R.H., Qi W. and Trail F. (2005) Eukaryotic Cell 4(11), 1926,1933.
79. Baker S.E., Perrone G., Richardson N.M., Gallo A. and Kubicek C.P. (2012) Microbiology 158, 147,154.
80. Hansen F.T., Sorensen J.L., Giese H., Sondergaard T.E. and Frandsen R.J.N. (2012) International Journal of Food Microbiology 155, 128,136.
81. Zaccaron A.Z., Woloshuk C.P. and Bluhm B.H. (2017) Fungal Biology 121(11), 966,983.
82. Sauer M., Lu P., Sangari R., Kennedy S., Polishook J., Bills G. and An Z. (2002) Mycology Research 106(4), 460,470.