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Ricardo De Nardi Fonoff 1 University of São Paulo “Luiz de Queiroz” College of Agriculture Exploring genetic biodiversity: secondary metabolites from Neotropical Annonaceae as a potential source of new pesticides Leandro do Prado Ribeiro Thesis presented to obtain the degree of Doctor in Science. Area: Entomology Piracicaba 2014 2 Leandro do Prado Ribeiro Agronomist Exploring genetic biodiversity: secondary metabolites from Neotropical Annonaceae as a potential source of new pesticides Advisor: Prof. Dr. JOSÉ DJAIR VENDRAMIM Thesis presented to obtain the degree of Doctor in Science. Area: Entomology Piracicaba 2014 Dados Internacionais de Catalogação na Publicação DIVISÃO DE BIBLIOTECA - DIBD/ESALQ/USP Ribeiro, Leandro do Prado Exploring genetic biodiversity: secondary metabolites from Neotropical Annonaceae as a potential source of new pesticides / Leandro do Prado Ribeiro. - - Piracicaba, 2014. 169 p: il. Tese (Doutorado) - - Escola Superior de Agricultura “Luiz de Queiroz”, 2014. 1. Aleloquímicos 2. Inseticidas botânicos 3. Acetogeninas 4. Fracionamentos biomonitorados 5. Técnicas cromatográficas I. Título CDD 641.41 R484e “Permitida a cópia total ou parcial deste documento, desde que citada a fonte -O autor” 3 “I offer this thesis to my family due to their support, understanding, and affection in every step of this challenge.” 4 5 ACKNOWLEDGEMENTS I wish to give thanks: To God – above all, my source of inspiration and enlightenment in every moment of my life. To Professor José Djair Vendramim for his guidance, support and sharing his expertise with me. Human and ethical senses are characteristics of Professor Djair on which I will base my future professional activities. To all professors from the Graduate Course in Entomology (ESALQ/USP) and employees from Department of Entomology and Acarology (LEA - ESALQ/USP). To the Research Foundation of São Paulo for the scholarship granted during my period in Brazil (grant number 2010/52638-0) and Canada (grant number 2013/02527-6). To National Science and Technology Institute for Biorational Control of Pest Insects, in especial to Professor João Batista Fernandes and his students (Ana Paula, Keylla, Leila, and Vanessa) for technical support and suggestions in the “chemical steps” of this study. To Dr. Sérgio Sartori from the Rare Fruits Brazilian Association (Rio Claro, SP, Brazil); Dr. José Bettiol Neto from the Fruit Center of the Agronomic Institute of Campinas (IAC/APTA, Jundiaí, SP, Brazil) and Vale Natural Reserve (Linhares, ES, Brazil) for the help with obtaining the Annonaceae species used in this study. I also thank Professor Renato Mello-Silva (Department of Botany, University of São Paulo (IB/USP) and the PhD. student Jenifer Carvalho Lopes for the help in the plant species location and their taxonomic identification and cataloging procedures. To Professors Pedro Takao Yamamoto, Italo Delalibera Junior, and Eduardo Micotti da Glória for the suport and permission to use their laboratory structures to conduct some steps of this study. Special thanks to colleagues Odimar, Luiz Henrique, Celeste and Mariana for their assistance, support, and friendship. To colleagues from Insect Plant Resistance and Insecticidal Plants Laboratory: Angelina Marcomini, Eliane Grisoto, Gabriel Gonçalves, Márcio Silva, Mônica Santos, Thiago Ansante for pleasant time and exchange of information and experiences during this period. Thanks in particular to Gabriel and Thiago for their assistance in conducting most part of this study. I also would like to thank to all 6 colleagues and friends from Department of Entomology and Acarology as well as my rommates Felipe and Aloísio. From Canada, I also would like to thank Professors Murray Isman and Yasmin Akhtar (The University of British Columbia - UBC) for their receptivity, support and shared knowledge during my experience abroad. Also thanks to my colleagues from UBC: Hoda, July, Jun, Mahnaz, Oriela, Rita and Viridiana, for their friendship and pleasant time. Special thanks to friends Rita and Gilson for their inconditional support in all stages of my experience in Canada. To all those who directly or indirectly contributed to the success of this work, my sincere thanks. 7 [...] Nunca deixe que lhe digam Que não vale a pena acreditar no sonho que se tem Ou que seus planos nunca vão dar certo Ou que você nunca vai ser alguém Tem gente que machuca os outros Tem gente que não sabe amar Mas eu sei que um dia a gente aprende Se você quiser alguém em quem confiar Confie em si mesmo QUEM ACREDITA SEMPRE ALCANÇA! “Mais uma vez – Renato Russo” (In Portuguese) 8 9 SUMMARY RESUMO....................................................................................................................13 ABSTRACT................................................................................................................15 INTRODUCTION…………………………………………………………………………...17 2 SEARCHING FOR POTENTIAL SOURCES OF GRAIN PROTECTORS IN EXTRACTS FROM NEOTROPICAL ANNONACEAE: SCREENING AND BIOGUIDED FRACTIONATIONS…………………………………………...……….23 Abstract……………………………………………………………………………………...23 2.1 Introduction...........................................................................................................23 2.2 Development…………………………………………………………….…..…………25 2.2.1 Material and methods………………………………………………………………..25 2.2.1.1 Species sampling and plant extract preparation (Step 1)………………….….25 2.2.1.2 Bioassays………………………………............................................................26 2.2.1.2.1 Screening for the identification of promising extracts (Step 2)……………….29 2.2.1.2.1.1 Evaluation of insecticidal activity……………………………...…………..…29 2.2.1.2.1.2 Evaluation of F1 progeny and damages…………………………...…...…….29 2.2.1.2.2 Concentration-response curves of active extracts ……………………..……30 2.2.1.2.3 Estimation of average lethal time (LT50) of the promising extracts …………30 2.2.1.2.4 Fungicidal and antiaflatoxigenic effects of the most promising extracts …30 2.2.1.3 Bioguided fractionations of active crude extracts (step 3)……………………....32 2.2.1.3.1 Partitioning of promising extracts……………………......................................32 2.2.1.3.1.1 Chemical profile of active partitions…………………………………………34 2.2.1.3.2 Fractionations of bioactive partitions………………………………………..…35 2.2.1.3.2.1 Hydroalcoholic partition from Annona mucosa seed extract……………...35 2.2.1.3.2.2 Hydroalcoholic partition from Annona sylvatica seed extract…………….35 2.2.1.3.2.3 Hexanic partition from Duguetia lanceolata leaf extract ……………….…36 2.2.1.3.3 Purification, isolation, and characterization of the major compound(s) from the most active fractions…………………………………………....................36 2.2.1.3.3.1 Major acetogenin from the most active fraction of Annona mucosa…….36 2.2.1.3.3.2 Major acetogenins from the purified fraction of Annona sylvatica……….37 2.2.1.3.3.3 Major compounds from the most active fraction of Duguetia lanceolata..37 2.2.1.4 Data analysis..................................................................................................38 2.2.2 Results and discussion……………………………………...................................39 10 2.2.2.1 Extraction yield (Step 1)…..............................................................................39 2.2.2.2 Selection of the promising crude extracts (Step 2)....………………..………..42 2.2.2.3 Estimation of lethal concentrations and average lethal time of the selected extracts…………………………………………………………………..…..….…54 2.2.2.4 Fungicidal and antiaflatoxigenic activity of the most promising extracts….…..54 2.2.2.5 Partitioning of promising extracts: yield and insecticidal activity (Step 3)…...62 2.2.2.5.1 Yield…………………………………………………………………………..…..62 2.2.2.5.2 Insecticidal activity of obtained partitions....................................................63 2.2.2.5.3 Chemical profile of active fractions……………………………………...….…67 2.2.2.6 Insecticidal activity of fractions obtained from the most active partitions..…..85 2.2.2.6.1 Fractions from hydroalcoholic partition of ethanolic extract of Annona mucosa seeds…………………………………………………………………..85 2.2.2.6.2 Purified fraction (rich in acetogenins) from hydroalcoholic partition of an ethanolic extract of Annona sylvatica seeds……………………….…......…86 2.2.2.6.3 Fractions from hexane partition of an ethanolic extract of Duguetia lanceolata leaves……………………………………………………………....86 2.2.2.7 Grain protective properties of isolate compounds from the most active fractions……………………………………………………………………...…….87 2.2.2.7.1 Majority acetogenin from the most active fraction of Annona mucosa….....87 2.2.2.7.2 Majority acetogenins from purified fraction of Annona sylvatica……………90 2.2.2.7.3 Majority compounds from the most active fraction of Duguetia lanceolata………………………………………………...……………..……...92 References…………………………………………………………………………..….…..96 3 COMPARATIVE BIOACTIVITY OF SELECTED SEED EXTRACTS FROM BRAZILIAN Annona SPECIES AND AN ACETOGENIN-BASED COMMERCIAL BIOINSECTICIDE AGAINST Brassica INSECT PESTS…………………………..105 Abstract…………………………………………………………………….....……………105 3.1 Introduction………………………………………………………...……………….....105 3.2 Development………………………………………………….…………….….……..108 3.2.1 Material and methods…………………………………….………………………..108 3.2.1.1 Annona crude seed extracts: sources and preparation…………..………….108 3.2.1.2 Test insects……………………………………………………..………………...108 3.2.1.3 Screening of Annona seed extracts in the laboratory……………..…………109 3.2.1.3.1 Oral toxicity bioassay…………………………………………..……..….……109 11 3.2.1.3.2 Contact toxicity bioassay………………………………..……………....…….109 3.2.1.3.3 Growth inhibition………………………………………………...……..………110 3.2.1.4 Aphicidal activity of
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