Cendawan entomopatogen sebagai penginduksi ketahanan tanaman: Sebuah tinjauan sistematis
Entomopathogenic fungi as plant resistance inducer: A systematic review
DOI:
https://doi.org/10.5994/jei.21.1.75Keywords:
characterization, entomopathogenic endophytic fungi, herbivorous insects, resistance induction, systemic resistanceAbstract
IInsect pathologists' attention to the potential of entomopathogenic fungi (EPF) as inducers of plant resistance has increased in recent years. Several types of EPF that have received attention as biocontrol agents for insect pest populations include Beauveria bassiana, Metarhizium anisopliae and Trichoderma sp. because they are able to infect and kill insects directly, has a wide host range, and has been used to control various types of insect pests. Apart from being able to infect and kill insect pests, EPF can also live endophytically in plant tissue and increase plant resistance to pest attacks. The presence of EPF as endophytes is able to induce plant resistance by stimulating an increase phytohormones production. In this article, we reviewed the role of fungi as entomopathogens, the characteristics of entomopathogenic fungi, and their role as inducers of plant resistance. The review was carried out by collecting information from original articles and related reports which reviewed the results of research on the role of entomopathogenic fungi as plant resistance inducers by including the keywords entomopathogenic endophytic fungi, resistance induction, characterization, systemic resistance and herbivorous insects. This systematic review concludes that EPF as an inducer of plant resistance is a very promising control alternative in the development of plant protection management against insect pests.
Downloads
References
Akello J, Sikora R. 2012. Systemic acropedal influence of endophyte seed treatment on Acyrthosiphon pisum and Aphis fabae offspring development and reproductive fitness. Biological Control. 61:215–221. DOI: https://doi.org/10.1016/j.biocontrol.2012.02.007.
Akello J, Dubois T, Coyne D, Kyamanywa S. 2008. Endophytic Beauveria bassiana in banana (Musa spp.) reduces banana weevil (Cosmopolites sordidus) fitness and damage. Crop protection. 27:1437–1441. DOI: https://doi.org/10.1016/j.cropro.2008.07.003.
Akutse K, Maniania N, Fiaboe K, Van Den Berg J, Ekesi S. 2013. Endophytic colonization of Vicia faba and Phaseolus vulgaris (Fabaceae) by fungal pathogens and their effects on the life-history parameters of Liriomyza huidobrensis (Diptera: Agromyzidae). Fungal Ecology. 6:293–301. DOI: https://doi.org/10.1016/j.funeco.2013.01.003.
Akutse KS, Kimemia JW, Ekesi S, Khamis FM, Ombura OL, Subramanian S. 2019. Ovicidal effects of entomopathogenic fungal isolates on the invasive fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal of Applied Entomology. 00:1–9. https://doi.org/10.1111/jen.12634.
Anwar W, Subhani MN, Haider MS, Shahid AA, Mushatq H, Rehman MZ. 2016. First record of Trichoderma longibrachiatum as entomopathogenic fungi against Bemisia tabaci in Pakistan. Pakistan Journal of Phytopathol. 28:287–294.
Ayudya DR, Herlinda S, Suwandi. 2019. Insecticidal activity of culture filtrates from liquid medium of Beauveria bassiana isolates from South Sumatra (Indonesia) wetland soil against larvae of Spodoptera litura. Biodiversitas. 20:2101–2109. DOI: https://doi.org/10.13057/biodiv/d200802.
Bamisile BS, Dash CK, Akutse KS, Keppanan R, Afolabi OG, Hussain M, Qasim M, Wang L. 2018. Prospects of endophytic fungal entomopathogens as biocontrol and plant growth promoting agents: an insight on how artificial inoculation methods affect endophytic colonization of host plants. Microbiological Research. DOI: https://doi.org/10.1016/j.micres.2018.08.016.
Berini F, Caccia S, Franzetti E, Congiu T, Marinelli F, Casartellic M, Tettamantia G. 2015. Effects of Trichoderma viride chitinases on the peritrophicmatrix of Lepidoptera. Pest Management Science. 2016:980–989. DOI https://doi.org/10.1002/ps.4078.
Biswas C, Dey P, Satpathy S, Satya P, Mahapatra B. 2013. Endophytic colonization of white jute (Corchorus capsularis) plants by different Beauveria bassiana strains for managing stem weevil (Apion corchori). Phytoparasitica. 41:17–21. DOI: https://doi.org/10.1007/s12600-012-0257-x.
Boomsma JJ, Jensen AB, Meyling NV dan Eilenberg J. 2014. Evolutionary interaction networks of insect pathogenic fungi. Annual Review of Entomology. 59:467–485. DOI: https://doi.org/10.1146/annurev-ento-011613-162054.
Boucias DG, Pendland JC, Latgé JP. 1988. Nonspecific factors involved in attachment of entomopathogenic deuteromycetes to host insect cuticle. Applied and Environmental Microbiology. 54:1795–1805. DOI: https://doi.org/10.1128/aem.54.7.1795-1805.1988.
Carneiro AA, Gomes EA, Guimarães CT, Fernandes FT, Cruz I. 2008. Molecular characterization and pathogenicity of isolates of Beauveria spp. to fall armyworm. Pesquisa Agropecuária Brasileira. 43:513–520. DOI: https://doi.org/10.1590/S0100-204X2008000400010.
Carvalhais LC, Dennis PG, Badri DV, Kidd BN, Vivanco JM, Schenk PM, 2015. Linking jasmonic acid signaling, root exudates, and rhizosphere microbiomes. Molecular Plant-Microbe Interactions. 28:1049–1058. DOI: https://doi.org/10.1094/MPMI-01-15-0016-R/.
Chapman RF. 1982. The Insect: Structure and Function. Cambridge: Hardvard University Press.
Clarkson JM, Charnley AK. 1996. New insights into the mechanisms of fungal pathogenesis in insects. Trends in Microbiology. 4:B197–203. DOI: https://doi.org/10.1016/0966-842X(96)10022-6.
Contreras-Cornejo HA, Macías-Rodríguez L, del-Val E, Larsen J. 2017. The root endophytic fungus Trichoderma atroviride induces foliar herbivory resistance in maize plants. Applied Soil Ecology. 124:45–53 DOI: https://doi.org/10.1016/j.apsoil.2017.10.004.
Dash CK, Bamisile BS, Keppanan R, Qasim M, Lin Y, Islam SUI, Hussain M, Wang L. 2018. Endophytic entomopathogenic fungi enhance the growth of Phaseolus vulgaris L. (Fabaceae) and negatively affect the development and reproduction of Tetranychus urticae koch (Acari: Tetranychidae). Microbial Pathogenesi. 125:385–392. DOI: https://doi.org/10.1016/j.micpath.2018.09.044.
Ekesi S, Adamu RS, Maniania NK. 2002. Ovicidal activity of entomopathogenic hyphomycetes to the legume pod borer, Maruca vitrata and the pod sucking bug Clavigralla tomentosicollis. Crop Protection. 21:589–595. DOI: https://doi.org/10.1016/S02612194(02)00015-7.
El-Sayed GN, Ignoffo CM, Leathers TD, Gupta SC. 1993a. Cuticular and non-cuticular substrate influence on expression of cuticle-degrading enzymes from conidia of entomopathogenic fungus, Nomuraea rileyi. Mycopathologia. 122:79–87. DOI: https://doi.org/10.1007/BF01103603.
El-Sayed GN, Ignoffo CM, Leathers TD, Gupta SC. 1993b. Insect cuticle and yeast extract effects on germination, growth, and production of hydrolytic enzymes by Nomuraea rileyi. Mycopathologia. 122:143–147. DOI: https://doi.org/10.1007/BF01103474.
Flawerina G, Trizelia, Nurbailis. 2021. Virulence of five isolates of indigenous Beauveria bassiana against eggs and nymphs of Bemisia tabaci gennadius (Hemiptera: Aleyrodidae). Current Agriculture Research Journal. 9:1–8. DOI: https://doi.org/10.12944/CARJ.9.1.07.
Garcia-Gutierrez C, MMB Gonzalez, MN Bautista. 2011. Patogenicidad de aislamientos de hongos entomopatógenos contra Spodoptera frugiperda (Lepidoptera: Noctuidae) y Epilachna varivestis (Coleoptera: Coccinellidae). Revista Colombiana de Entomología. 37:217–222. DOI: https://doi.org/10.25100/socolen.v37i2.9077.
Gathage JW, Lagat ZO, Fiaboe KKM, Akutse KS, Ekesi S, Maniania NK. 2016. Prospects of fungal endophytes in the control of Liriomyza leafminer flies in common bean Phaseolus vulgaris under field conditions. BioControl. 61:741–753. DOI: https://doi.org/10.1007/s10526-016-9761-0.
Giridhar D, Ravi SN, Kirian KV, Kartheek D, Rajanikanth P, Nagalakshmi DM. 2012. Purification, characterization and antifungal activity of chitinase from Trichoderma viride N9. Cell and Tissue Research. 12:3187–3192.
Gómez I, Ocelotl J, Sánchez J, Lima C. 2018. Enhancement of Bacillus thuringiensis Cry1Ab and Cry1Fa toxicity to Spodoptera frugiperda by domain iii mutations indicates there are two limiting steps in toxicity as defined by receptor binding and protein stability. Applied and Environmental Microbiology. 84:e01393-18. DOI: https://doi.org/10.1128/AEM.01393-18.
González-Mas N, Cuenca-Medina M, Gutiérrez-Sánchez F, Quesada-Moraga E. 2019a. Bottom-up effects of endophytic Beauveria Bassiana on multitrophic interactions between the cotton aphid, Aphis gossypii, and its natural enemies in melon. Journal of Pest Science. 92:1271–1281. DOI: https://doi.org/10.1007/s10340-019-01098-5.
González-Mas N, Sánchez-Ortiz A, Valverde-García P, Quesada-Moraga E. 2019b. Effects of endophytic entomopathogenic ascomycetes on the life-history traits of Aphis gossypii Glover and its interactions with melon plants. Insects. 10:165. DOI: https://doi.org/10.3390/insects10060165.
Greenfield M, Gómez-Jiménez MI, Ortiz V, Vega FE, Kramer M, Parsa S. 2016. Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation. Biological Control. 95:40–48. DOI: https://doi.org/10.1016/j.biocontrol.2016.01.002.
Gurulingappa P, Sword GA, Murdoch G, Mcgee PA. 2010. Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. Biological Control. 55:34–41. DOI: https://doi.org/10.1016/j.biocontrol.2010.06.011.
Hajek AE, Gryganskyi A, Bittner T, Liebherr JK, Liebherr JH. 2016. Phylogenetic placement of two species known only from resting spores: Zoophthora independentia sp. nov. and Z. portericomb. nov. (Entomophthorales: Entomophthoraceae). Journal of Invertebrate Pathology. 140:68–74. https://doi.org/10.1016/j.jip.2016.09.002.
Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A. 2015. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews. 79:293–320 DOI: https://doi.org/10.1128/mmbr.00050-14.
Hendra Y, Trizelia, Syahrawati M. 2022. Aplikasi cendawan entomopatogen Beauveria bassiana (Bals.) pada tanaman padi dan pengaruhnya terhadap preferensi oviposisi imago wereng batang coklat (Nilaparvata lugens Stal). Proceedings Series on Physical & Formal Sciences. 4:475–481. DOI: https://doi.org/10.30595/pspfs.v4i.539.
Herlinda S, Gustianingtyas M, Suwandi, Suharjo R, Sari JMP, Suparman, Hamidson H, Hasyim H. 2022. Endophytic fungi from South Sumatra (Indonesia) in seed-treated corn suppressing Spodoptera frugiperda growth. Biodiversitas. 23:6013-6020. DOI: https://doi.org/10.13057/biodiv/d231156.
Humber RA. 2008. Evolution of entomopathogenicity in fungi. Journal of Invertebrate Pathology. 98:262e266. DOI: https://doi.org/10.1016/j.jip.2008.02.017.
Jaber LR, Araj SE. 2018. Interactions among endophytic fungal entomopathogens (Ascomycota: Hypocreales), the green peach aphid Myzus persicae Sulzer (Homoptera: Aphididae), and the aphid endoparasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Biological Control. 116:53–61. DOI: https://doi.org/10.1016/j.biocontrol.2017.04.005.
Jaber LR, Enkerli J. 2016. Effect of seed treatment duration on growth and colonization of Vicia faba by endophytic Beauveria bassiana and Metarhizium brunneum. Biological Control. 103:187–195. DOI: https://doi.org/10.1016/j.biocontrol.2016.09.008.
Jallow MF, Dugassa-Gobena D, Vidal S. 2008. Influence of an endophytic fungus on host plant selection by a polyphagous moth via volatile spectrum changes. Arthropod-Plant Interactions. 2:53-62. DOI: https://doi.org/10.1007/s11829-008-9033-8.
Kessler A, Baldwin IT. 2002. Plant responses to insect herbivory: The emerging molecular analysis. Annual Review of Plant Biology. 53: 299–328. DOI: https://doi.org/10.1146/annurev.arplant.53.100301.135207.
Steinbrenner AD, Muñoz-Amat KF, Mehrkhou F, Mahmoudian M, Ghosta Y. 2018. Pathogenicity of three different entomopathogenic fungi, Metarhizium anisopliae IRAN 2252, Nomuraea rileyi IRAN 1020C and Paecilomyces tenuipes IRAN 1026C against the potato tubermoth, Phthorimaea operculella Zeller (Lepidoptera: Gelechiidae). Potato Research. 61:297–308. DOI: https://doi.org/10.1007/s11540-018-9378-z.
Kim J, Felton GW. 2013. Priming of antiherbivore defensive responses in plants. Insect Science. 20: 273–285. DOI: https://doi.org/10.1111/j.1744-7917.2012.01584.x.
Klieber J, and Reineke A. 2016. The entomopathogen Beauveria bassiana has epiphytic and endophytic activity against the tomato leaf miner Tuta absoluta. Journal of Applied Entomology. 140:580–589. DOI: https://doi.org/10.1111/jen.12287.
Kumar V, Singh GP, Kumar V, Babu AM, Datta RK. 1997. SEM study on the invasion of Nomuraea rileyi (Farlow) on silkworm, Bombix mori Linn. causing green muscardine. Mycopathologia. 139:141–144. DOI: https://doi.org/10.1023/A:1006800231647.
Lira AC, Mascarin GM, Júnior ID. 2020. Microsclerotia production of Metarhizium spp. for dual role as plant biostimulant and control of Spodoptera frugiperda through corn seed coating. Fungal Biology. 124:689-699. DOI: https://doi.org/10.1016/j.funbio.2020.03.011.
Lopez DC, Zhu-Salzman K, Ek-Ramos MJ, Sword GA. 2014. The entomopathogenic fungal endophytes Purpureocillium lilacinum (formerly Paecilomyces lilacinus) and Beauveria bassiana negatively affect cotton aphid reproduction under both greenhouse and field conditions. PloS One. 9:e103891. DOI: https://doi.org/10.1371/journal.pone.0103891.
Manoussopoulos Y, Mantzoukas S, Lagogiannis I, Goudoudaki S, Kambouris M. 2019. Effects of three strawberry entomopathogenic fungi on the prefeeding behavior of the Aphid Myzus persicae. Journal of Insect Behavior. 32:99–108. DOI: https://doi.org/10.1007/s10905-019-09709-w/.
Mantzoukas S, Grammatikopoulos G. 2020. The effect of three entomopathogenic endophytes of the sweet sorghum on the growth and feeding performance of its pest, Sesamia nonagrioides larvae, and their efficacy under field conditions.Crop Protection. 127:104952. DOI: https://doi.org/10.1016/j.cropro.2019.104952.
Martinuz A, Schouten, A, Menjivar R, Sikora R. 2012. Effectiveness of systemic resistance toward Aphis gossypii (Homoptera: Aphididae) as induced by combined applications of the endophytes Fusarium oxysporum Fo162 and Rhizobium etli G12. Biological Control. 62:206–212. DOI: https://doi.org/10.1016/j.biocontrol.2012.05.006.
Moisan K, Cordovez V, Van de Zande EM, Raaijmakers JM, Dicke M, Lucas-Barbosa D. 2019. Volatiles of pathogenic and non-pathogenic soilborne fungi affect plant development and resistance to insects. Oecologia. 190:589–604. DOI: https://doi.org/10.1007/s00442-019-04433-w.
Muvea AM, Meyhöfer R, Subramanian S, Poehling HM, Ekesi S, Maniania NK. 2014. Colonization of onions by endophytic fungi and their impacts on the biology of Thrips tabaci. PloS One. 9:e108242. DOI: https://doi.org/10.1371/journal.pone.0108242.
Nunes ARF, Martins JN, Furlaneto MC, Barros NM. 2010. Production of cuticle egrading proteases by Nomuraea rileyi and its virulence against Anticarsia gemmatalis. Ciência Rural. 40:1853–1859. DOI: https://doi.org/10.1590/S0103-84782010005000149.
Nunilahwati H, Herlinda S, Irsan C, Pujiastuti Y. 2012. Exploration, isolation and selection entomopathogenic fungi infectious to Plutella xylostella (Lepidoptera: Yponomeutidae) on green mustard (Brassica chinensis) crop in South Sumatra. Jurnal HPT Tropika. 12:1–11. DOI: https://doi.org/10.23960/j.hptt.1121-11.
Opisa S, du Plessis H, Akutse KS, Fiaboe KKM, Ekesi S. 2018. Effects of entomopathogenic fungi and Bacillus thuringiensis‐based biopesticides on Spoladea recurvalis (Lepidoptera: Crambidae). Journal of Applied Entomology. 142:617–626. DOI: https://doi.org/10.1111/jen.12512.
Orole O, Adejumo T. 2009. Activity of fungal endophytes against four maize wilt pathogens. African Journal of Microbiology Research. 3:969–973.
Peng Y, Li SJ, Yan J, Tang Y, Cheng JP, Gao AJ, Yao X, Ruan JJ, Xu BL. 2021. Research progress on phytopathogenic fungi and their role as biocontrol agents. Frontiers in Microbiology. 12:670135. DOI: https://doi.org/10.3389/fmicb.2021.670135.
Pires LM, Marques EJ, Wanderley‐Teixeira V, Teixeira ÁA, Alves LC, Alves ESB. 2009. Ultrastructure of Tuta absoluta parasitized eggs and the reproductive potential of females after parasitism by Metarhizium anisopliae. Micron. 40:255–261. DOI: https://doi.org/10.1016/j.micron.2008.07.00.8.
Powell WA, Klingeman WE, Ownley BH, Gwinn KD. 2009. Evidence of endophytic Beauveria bassiana in seed-treated tomato plants acting as a systemic entomopathogen to larval Helicoverpa zea (Lepidoptera: Noctuidae). Journal of Entomological Science. 44:391–396. DOI: https://doi.org/10.18474/0749-8004-44.4.391.
Prayogo Y, Bayu MSYI, Indiati SW, Harnowo D, Mejaya MJ. 2022a. Biopesticide efficacy against main pests, diseases, and natural enemies of mungbean (Vigna Radiata L.). Applied Ecology and Environmental Research. 20:931–945. DOI: https://doi.org/10.15666/aeer/2002_931945.
Prayogo Y, Bayu MSYI, Indiati SW, Sumartini, Indriani FC, Ginting E, Susanto GWA, Harnowo D, Mejaya MJ. 2024. Eco-friendly biopesticide of Beauveria Bassiana to control sweet potato weevil Cylas formicarius (Coleoptera: Curculionidae). IOP Conference Series: Earth and Environmental Science. 1312:012025. DOI: https://doi.org/10.1088/1755-1315/1312/1/012025.
Prayogo Y, Bayu MSYI, Indiati SW, Sumartini, Mejaya MJ, Harnowo D, Susanto GWA, Baliadi Y. 2022b. Innovation of main pest and disease control technology using biopesticides on soybean (Glycine max L.). Applied Ecology and Environmental Research. 21:589–608. DOI: https://doi.org/10.15666/aeer/2101_589608.
Prayogo Y, Bayu MSYI, Indiati SW, Sumartini, Susanto GWA, Harnowo D, Baliadi Y, Widiarta IN, Harsono A, Budiono R, Mejaya MJ, Supriadi, K. 2022. Control measure of sweet potato weevil (Cylas Formicarius Fab.) (Coleoptera: Curculionidae) in endemic land of entisol type using mulch and entomopathogenic fungus Beauveria bassiana. Open Agriculture. 8:20220237. DOI: https://doi.org/10.1515/opag-2022-0237.
Quesada-Moraga E, Munoz-Ledesma F, Santiago-Alvarez C. 2009. Systemic protection of Papaver somniferum L. against Iraella uteipes (Hymenoptera: Cynipidae) by an endophytic strain of Beauveria bassiana (Ascomycota: Hypocreales). Environmental Entomology. 38:723–730. DOI: https://doi.org/10.1603/022.038.0324.
Ramirez‐Rodriguez D, Sánchez‐Peña SR. 2016. Endophytic Beauveria bassiana in Zea mays: Pathogenicity against larvae of fall army-worm Spodoptera frugiperda. Southwestern Entomologist. 41:875–878. DOI: https://doi.org/10.3958/059.041.0330.
Resquín-Romero G, Garrido-Jurado I, Delso C, Ríos-Moreno A, Quesada-Moraga E. 2016. Transient endophytic colonizations of plants improve the outcome of foliar appliations of mycoinsecticides against chewing insects. Journal of Invertebrate Pathology. 136:23–31. DOI: https://doi.org/10.1016/j.jip.2016.03.003.
Rodríguez-González Á, Mayo S, González-López Ó, Reinoso B, Gutierrez S, Casquero PA. 2017. Inhibitory activity of Beauveria bassiana and Trichoderma spp. on the insect pests Xylotrechus arvicola (Coleoptera: Cerambycidae and Acanthoscelides obtectus (Coleoptera: Chrisomelidae: Bruchinae). Environmental Monitoring and Assessment. 189:12–20. DOI: https://doi.org/10.1007/s10661-016-5719-z.
Rodriguez RJ, White JF, Arnold AE, Redman R. 2009. Fungal endophytes: diversity and functional roles. New Phytologist. 182:314–330. DOI: https://doi.org/10.1111/j.1469-8137.2009.02773.x.
Rodriguez-Saona C, Chalmers JA, Raj S, Thaler JS. 2010. Induced plant responses to multiple damagers: Differential effects on an herbivore and its parasitoid. Oecologia. 143:566–577. DOI: https://doi.org/10.1007/s00442-005-0006-7.
Rondot Y, Reineke A. 2018. Endophytic Beauveria bassiana in grapevine Vitis vinifera (L.) reduces infestation with piercing-sucking insects. Bio Control. 116:82–89. DOI: https://doi.org/10.1016/j.biocontrol.2016.10.006.
Russo SA, Pelizza MF, Vianna N, Allegrucci MN, Cabello AV, Toledo C, Mourelos AC, Scorsetti. 2018. Effect of endophitic entomopathogenic fungi on soybean Glycine max (L.) Merr. Growth and yield. Journal of King Saud University –Science. 31:728–736. DOI: https://doi.org/10.1016/j.jksus.2018.04.008.
Russo ML, Scorsetti AC, Vianna MF, Allegrucci N, Ferreri NA, Cabello MN, Pelizza SA. 2019. Effects of endophytic Beauveria bassiana (Ascomycota: Hypocreales) on biological, reproductive parameters and food preference of the soybean pest Helicoverpa gelotopoeon. Journal of King Saud University - Science. 31:1077–1082. DOI: https://doi.org/10.1016/j.jksus.2018.11.009.
Salas-Marina MA, Isordia-Jasso MI, Islas-Osuna, MA, Delgado-Sánchez P, Jiménez-Bremont JF, Rodríguez-Kessler M, Rosales-Saavedra MT, Herrera-Estrella A, Casas-Flores S. 2015. The Epl1 and Sm1 protein from Trichoderma atroviride and Trichoderma virens differentially modulate systemic disease resistance against different life style pathogens in Solanum lycopersicum. Frontiers in Plant Science. 6:77. DOI: https://doi.org/10.3389/fpls.2015.00077.
Sánchez-Rodríguez AR, Raya-Díaz S, Zamarreño ÁM, García-Mina JM, Del Campillo MC, Quesada-Moraga E. 2017. An endophytic Beauveria bassiana strain increases spike production in bread and durum wheat plants and effectively controls cotton leafworm (Spodoptera littoralis) larvae. Biological Control. 116:90–102. DOI: https://doi.org/10.1016/j.biocontrol.2017.01.012.
Saragih M, Nurbailis, Trizelia, Yusniwati. 2021. Aplikasi cendawan Beauveria bassiana melalui perendaman benih dan pengaruhnya terhadap kolonisasi dan kandungan klorofil daun tanaman cabai merah (Capsicum annuum L.). Jurnal Pertanian Tropik. 8:107–116. DOI: https://doi.org/10.32734/jpt.v8i2.6519.
Saragih M, Trizelia, Nurbailis, Yusniwati. 2019a. Endophytic colonization and plant growth promoting effect by entomopathogenic fungus, Beauveria bassiana to red chili (Capsicum annuum L.) with different inoculation methods. IOP Conference Series: Earth and Environmental Science. 305:012070. DOI: https://doi.org/10.1088/1755-1315/305/1/012070.
Saragih M, Trizelia, Nurbailis, Yusniwati. 2019b. Uji potensi cendawan endofit Beauveria bassiana terhadap perkecambahan dan pertumbuhan bibit tanaman cabai merah (Capsicum annuum L.). Unri Conference Series: Agriculture and Food Security. 1:151–159. DOI: https://doi.org/10.31258/unricsagr.1a20.
Saragih M, Trizelia, Nurbailis, Yusniwati. 2022. Effect of colonization of the fungus Beauveria bassiana on salicylic acid content and population of Bemisia tabaci on red chili (Capsicum annuum l.). 17:1119-1128. DOI: https://doi.org/10.5281/zenodo.7003536.
Sari JMP, Herlinda S, Suwandi. 2022. Endophytic fungi from South Sumatra (Indonesia) in seed-treated corn seedlings Afecting development of the fall armyworm, Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae). Egyptian Journal of Biological Pest Control. 32:103. DOI: https://doi.org/10.1186/s41938-022-00605-8.
Seidl V. 2008. Chitinases of filamentous fungi: A large group of diverse proteins with multiple physiological functions. Fungal Biology Reviews. 22:36–42. DOI: https://doi.org/10.1016/j.fbr.2008.03.002.
Shahid AA, Rao QA, Bakhsh A, Husnain T. 2012. Entomopathogenic fungi as biological controllers: New insights into their virulence and pathogenicity. Archives of Biological Sciences. 64:21–42. DOI: https://doi.org/10.2298/ABS1201021S.
Singh S, Kaur I, Kariyat R. 2021. The multifunctional roles of polyphenols in plant-herbivore interactions. International Journal of Molecular Sciences. 22:1442. DOI: https://doi.org/10.3390/ijms22031442.
Skovgård H, Steenberg T. 2002. Activity of pupal parasitoids ofthestablefly Stomoxys calcitrans and prevalence of entomopathogenic fungi in the stable fly and the house fly Musca domestica in Denmark. BioControl. 47:45–60. DOI: https://doi.org/10.1023/A:1014434004946.
Smith RJ, Pekrul S, Grula E. 1981. Requirement for sequential enzymatic activities for penetration of the integument of the corn earworm (Heliothis zea). Journal of Invertebrate Pathology. 38: 335–344. DOI: https://doi.org/10.1016/0022-2011(81)90099-9.
Srisukchayakul P, Wiwat C, Pantuwatana S. 2005. Studies on the pathogenesis of the local isolates of Nomuraea rileyi against Spodoptera litura. ScienciaAsia. 31:273–276. DOI: https://doi.org/10.2306/scienceasia1513-1874.2005.31.273.
Steenberg T, Jespersen JB, Jensen KMV, Nielsen BO, Humber RA. 2001. Entomopathogenic fungi in flies associated withpastured cattle in Denmark. Journal of Invertebrate Pathology. 77:186–197. DOI: https://doi.org/10.1006/jipa.2001.5021.
Thomas P, Sekhar AC. 2014. Live cell imaging reveals extensive intra cellular cytoplasmic colonization of banana by normally noncultivable endophytic bacteria. AOB Plants 6:plu002. DOI: https://doi.org/10.1093/aobpla/plu002.
Trizelia. 2020. The effect of seed treatment duration with entomopathogenic fungi Beauveria bassiana on seed germination and seedling growth of chili. JERAMI: Indonesian Journal of Crop Science. 3:25–29. DOI: https://doi.org/10.25077/jijcs.3.1.25-29.2020.
Trizelia, Nurdin F. 2010. Virulence of Entomo-pathogenic Fungus Beauveria bassiana isolates to Crocidolomia pavonana F (Lepidoptera: Crambidae). Agrivita. 32:254–260. DOI: https://doi.org/10.23960/j.hptt.213151-158.
Trizelia, Nurbailis, Ernawati D. 2013. Virulensi berbagai isolat jamur entomopatogen Metarhizium spp. terhadap hama penggerek buah kakao Conopomorpha Cramerella Snell. (Lepidoptera: Gracillariidae). Jurnal HPT Tropika. 13:151–158.
Trizelia, Rahma H, Martinius. 2021. Selection of endophytic fungi from Shallot that potential as entomopathogens on Tenebrio molitor and Spodoptera litura larvae. Journal of Biopesticides. 14:125–131. DOI: https://doi.org/10.57182/jbiopestic.14.2.125-131.
Trizelia, Rahma H, Syahrawati M. 2023a. Virulance of five isolates of the entomopathogenic fungus, Metarhizium anisopliae, against brown planhopper (Nillaparvata lugens). Jurnal Proteksi Tanaman. 7:127–135. DOI: https://doi.org/10.25077/jpt.7.2.127-133.2023.
Trizelia, Rahma H, Syahrawati M. 2023b. Diversity of endophytic fungi of rice plants in Padang City, Indonesia, entomopathogenic to brown planthopper (Nilaparva talugens). Biodiversitas. 24:2384–2391. DOI: https://doi.org/10.13057/biodiv/d240453.
Trizelia, Reflin, Ananda W. 2016. Virulensi beberapa isolat cendawan entomopatogen endofit Beauveria bassiana Bals. terhadap Spodoptera litura F. (Lepidoptera: Noctuidae). In: Ismadi et al. (Eds.), Prosiding Seminar Nasional BKS PTN Wilayah Barat Bidang Ilmu Pertanian (Lhokseumawe, 4-6 Agustus 2016). pp. 409–415. Lhokseumawe: Universitas Malikussaleh
Trizelia, Sulyanti, Saputra R. 2020. Kemampuan kolonisasi cendawan endofit Trichoderma sp. dan Beauveria bassiana pada tanaman cabai dan pengaruhnya terhadap populasi kutu daun Myzus persicae. In: Seminar Nasional Fakultas Pertanian UPN “Veteran” (Yogyakarta, 14 Oktober 2020). pp. 188–198. Yogyakarta: UPN Veteran.
Trizelia, Syahrawati M, Mardiah A. 2011. Patogenisitas beberapa isolat cendawan entomopatogen Metarhizium spp. terhadap telur Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Jurnal Entomologi Indonesia. 8:45–54. DOI: https://doi.org/10.5994/jei.8.1.45.
Trizelia, Yanti Y, Suhriani. 2019. Potensi cendawan entomopatogen Beauveria bassiana (Bals.) untuk pengendalian kepik kubis Eurydema pulchrum Westw. (Hemiptera: Pentatomidae). In: Prosiding Seminar Nasional Agroteknologi 2019 Jurusan Agroteknologi Universitas Islam Negeri Sunan Gunung Djati (Bandung, 2 Maret 2019) pp. 346-352. Bandung: Universitas Islam Negeri Sunan Gunung Djati.
Vadassery J, Reichelt M, Hause B, Gershenzon J, Boland W, Mithöfer A. 2012. CML42-mediated calcium signaling coordinates responses to Spodoptera herbivory and abiotic stresses in Arabidopsis. Plant Physiology. 159:1159–1175. DOI: https://doi.org/10.1104/pp.112.198150.
Van der Does D, Leon-Reyes A, Koornneef A, Van Verk MC, Rodenburg N, Pauwels L, Goossens A, Körbes AP, Memelink J, Ritsema T, Van Wees SCM, Pieterse CMJ. 2013. Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. The Plant Cell. 25:744–761. DOI: https://doi.org/10.1105/tpc.112.108548.
Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Koike M, Maniania NK, Monzon A, Ownley BH. 2009. Fungal entomopathogens: New insights on their ecology. Fungal Ecology. 2:149–159. DOI: https://doi.org/10.1016/j.funeco.2009.05.001.
Vega FE, Meyling NV, Luangsa-Ard JJ, Blackwell M. 2012. Chapter 6–Fungal Entomopathogens. In: Vega FE, Kaya HK (Eds.) Insect Pathology. 2nd ed. pp. 171–220. San Diego: Academic Press. DOI: https://doi.org/10.1016/B978-0-12-384984-7.00006-3.
Vega FE. 2008. Insect pathology and fungal endophytes. Journal of Invertebrate Pathology. 98:277–279. DOI: https://doi.org/10.1016/j.jip.2008.01.008.
Vega FE. 2018. The use of fungal entomopathogens as endophytes in biological control: A review. Mycologia. 110:4–30. DOI: https://doi.org/10.1080/00275514.2017.1418578.
Vidal S, Jaber LR. 2015. Entomopathogenic fungi as endophytes: Plant endophyte herbivore interactions and prospects for use in biological control. Current Science 109:46–54.
Verhage A, Vlaardingerbroek I, Raaymakers C, Van Dam NM, Dicke M, Van Wees SCM, Pieterse CMJ. 2011. Rewiring of the jasmonate signaling pathway in Arabidopsis during insect herbivory. Frontiers in Plant Science. 2:42. DOI: https://doi.org/10.3389/fpls.2011.00047.
Villacorta A. 1983. Ovicidal activity of Metarhizium anisopliae isolate CM‐14 on the coffee leaf miner. Perileucoptera coffeella (Lepidoptera: Lyonetiidae). Entomophaga. 28:179–184. DOI: https://doi.org/10.1007/BF02372142.
White JF, Belanger F, Meyer W, Sullivan RF, Bischoff JF, Lewis E.A. 2002. Clavicipitalean fungal epibionts and endophytes—development of symbiotic interactions with plants. Symbiosis. 33:201–213.
White JF, Torres MS, Somu MP, Johnson H, Irizarry I, Chen Q, Zhang N, Walsh E, Tadych M, Bergen MS. 2014. Hydrogen peroxide staining to visualize intracellular bacterial infections of seedling root cells. Microscopy Research and Technique. 77:566–573. DOI: https://doi.org/10.1002/jemt.22375.
White MM, Lichtwardt RW, Colbo MH. 2006. Confirmation and identification of parasitic stages of obligate endobionts (Harpellales) in blackflies (Simuliidae) by means of rRNA sequence data. Mycological Research. 110:1070–1079. DOI: https://doi.org/10.1016/j.mycres.2006.06.008.
Yuliana A, Trizelia, Sulyanti. 2023. Aplikasi cendawan entomopatogen beauveria bassiana pada benih bawang merah dan pengaruhnya terhadap perkecambahan dan pertumbuhan bibit. Jurnal Sains Agro. 8:88–96. DOI: https://doi.org/10.36355/jsa.v8i2.1164.
Yusniwati, Nurbailis, Trizelia, Saragih M. 2023a. Potency of entomopathogen Beauveria bassiana fungus as biofertilizer and biostimulant to increase the plant growth of Cayenne pepper (Capsicum frutescens L.). IOP Conference Series: Earth and Environmental Science. 1160:012005. DOI: https://doi.org/10.1088/1755-1315/1160/1/012005.
Yusniwati, Trizelia, Nurbailis, Saragih. 2023b. Profile and bioactivity of bioactive compounds of Beauveria bassiana fungi entomopathogens of endophytes as plant growth boosters. Agrium: Jurnal Ilmu Pertanian. 26:50–56. DOI: https://doi.org/10.30596/agrium.v26i1.14364.
Zebelo SA, Matsui K, Ozawa R, Maffei ME. 2012. Plasma membrane potential depolarization and cytosolic calcium flux are early events involvedin tomato (Solanum lycopersicon) plant-to-plant communication. Plant Science. 196:93–100. DOI: https://doi.org/10.1016/j.plantsci.2012.08.006.
Zhang L, Shi WB, Feng MG. 2014. Histopathological and molecular insights into the ovicidal activities of two entomopathogenic fungi against two‐spotted spidermite. Journal of Invertebrate Pathology. 117:73–78. DOI: https://doi.org/10.1016/j.jip.2014.02.005.
Zhu-Salzman K, Luthe DS, Felton GW. 2008. Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiology. 146:852–858. DOI: https://doi.org/10.1104/pp.107.112177.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Indri Yanil Vajri, Trizelia, Retna Astuti Kuswardani, Magdalena Saragih
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).