Diversity and Abundance of Soil Collembola during GM Rice Overexpressing Cry1B-Cry1Aa Cultivations at Four Confined Field Trials in West Java

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Yayuk Rahayuningsih Suhardjono
Amy Estiati
Syamsidah Rahmawati
Satya Nugroho


Collembola (springtails) is an important soil biology indicator to monitor toxicity or ecological disturbances in the ecosystem. The impact of Bacillus thuringiensis (Bt) rice cv Rojolele events expressing Cry1B-Cry1Aa driven by the maize ubiquitin promoter resistant to yellow rice stem borer (YSB, Scirpophaga incertulas Walker) on non-target Collembola community was assessed. The experiment was performed at four locations under confined field trials according to the Indonesia’s environmental safety regulation on genetically engineered crops. Six transgenic rice events were tested with non-transgenic Rojolele and the moderately resistant IR42 rice varieties as controls. The experimental design was randomised block design with three replicates. Collembola were collected from the bunds between plots using pitfall and Berlese funnel traps at seedling, vegetative and generative stages, as well as at harvesting time. The results showed that Collembola abundance and diversity were significantly affected by both experimental sites and observation times. However, no significant differences in Collembola diversity and abundance between Bt rice and non-Bt controls were observed. Thus, we can conclude that the cultivation of the Bt rice cv Rojolele events expressing Cry1B-Cry1Aa protein fusion do not adversely affect biodiversity and abundance of Collembola at the four confined rice fields.

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Diversity and Abundance of Soil Collembola during GM Rice Overexpressing Cry1B-Cry1Aa Cultivations at Four Confined Field Trials in West Java. (2022). Tropical Life Sciences Research, 33(3), 85–106. https://doi.org/10.21315/tlsr2022.33.3.6
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Arias-martín M, García M, José M, Ortego F, Castañera P, and Farinós G P. (2016). Agriculture, ecosystems and environment effects of three-year cultivation of Cry1Ab-expressing Bt maize on soil microarthropod communities. Agriculture, Ecosystems and Environment 220: 125–134. https://doi.org/10.1016/j.agee.2015.09.007

Bai Y Y, Yan R H, Ye G Y, Huang F N and Cheng J A. (2010). Effects of transgenic rice expressing Bacillus thuringiensis Cry1Ab protein on ground-dwelling Collembolan community in postharvest seasons. Environmental Entomology 39(1): 243–251. https://doi.org/10.1603/en09149

Bitzer R J, Rice M E, Pilcher C D, Pilcher C L and Lam W K F. (2005). Biodiversity and community structure of epedaphic and euedaphic springtails (Collembola) in transgenic rootworm Bt corn. Environmental Entomology 34(5): 1346–1376. https://doi.org/10.1093/ee/34.5.1346

Bravo A. (1997). Phylogenetic relationships of Bacillus thuringiensis ?-endotoxin family proteins and their functional domains. Journal of Bacteriology 179(9): 2793–2801. https://doi.org/10.1128/jb.179.9.2793-2801.1997

Breitler J C, Vassal J M, Del Mar Catala M, Meynard D, Marfà V, Melé E, Royer M, Murillo I, San Segundo B, Guiderdoni E, and Messeguer J. (2004). Bt rice harbouring cry genes controlled by a constitutive or wound-inducible promoter: Protection and transgene expression under Mediterranean field conditions. Plant Biotechnology Journal 2(5): 417–430. https://doi.org/10.1111/j.1467-7652.2004.00086.x

Chen Y, Tian J C, Shen Z C, Peng Y F, Hu C, Guo Y Y and Ye G Y. (2010). Transgenic rice plants expressing a fused protein of Cry1Ab/Vip3H has resistance to rice stem borers under laboratory and field conditions. Journal of Economic Entomology 103(4): 1444–1453. https://doi.org/10.1603/ec10014

Estiati A and Herman M. (2016). Biosafety regulation of genetically modified products in Indonesia. Analisis Kebijakan Pertanian 13(2): 129–146. https://doi.org/10.21082/akp.v13n2.2015.129-146

Filser J. (2002). Role of Collembola in C and N cycling. Proceedings of the Xth International Colloquium on Apterygota, ?eské Bud?jovice 2000: Apterygota at the Beginning of the Third Millennium. Pedobiologia, 234–245. https://doi.org/https://doi.org/10.1078/0031-4056-00130

Ho N H, Baisakh N, Oliva N, Datta K, Frutos R and Datta S K. (2006). Translational fusion hybrid Bt genes confer resistance against yellow stem borer in transgenic elite Vietnamese rice (Oryza sativa L.) cultivars. Crop Science 46: 781–789. https://doi.org/10.2135/cropsci2005.06-0111

Indriyati and Wibowo L. (2008). Keragaman dan kemelimpahan Collembola serta Arthropoda tanah di lahan sawah organik dan konvensional pada masa bera. Jurnal Hama Dan Penyakit Tumbuhan Tropika 8(2): 110–116. https://doi.org/10.23960/j.hptt.28110-116

International Service for the Acquisition of Agri-biotech Applications (ISAAA). (2018). Global status of commercialized biotech/GM crops in 2018. ISAAA Brief No. 54.

Kumar S. (2014). Biosafety issues of genetically modified organisms. Biosafety 3(2): 2–3. https://doi.org/10.4172/2167-0331.1000e150

Lavelle P and Spain A V. (2001). Soil ecology. New York: Kluwer Academic Publisher, 385–460. https://doi.org/10.1007/978-94-017-5279-4

Lee Q and Widden P. (1996). Folsomia candida, a “fungivorous” collembolan, feeds preferentially on nematodes rather than soil fungi. Soil Biology and Biochemistry 28: 689–690.

Liu Q, Hallerman E, Peng Y and Li Y. (2016). Development of Bt rice and Bt maize in China and their efficacy in target pest control. International Journal of Molecular Sciences 17(10): 1–15. https://doi.org/10.3390/ijms17101561

Ludwig J A and Reynolds J F. (1988). Statistical ecology: A primer on methods and computing (Vol. 2). New York: John Wiley & Sons; Inc.

Makkar G S and Bentur J S. (2017). Breeding for stem borer and gall midge resistance in rice. In R Arora and S Sandhu (Eds.), Breeding insect resistant crops for sustainable agriculture. Singapore: Springer, 323–352.

Mendelsohn M, Kough J, Vaituzis Z and Matthews K. (2003). Are Bt crops safe ? Nature Biotechnology 21(9): 1003–1009. https://doi.org/10.1038/nbt0903-1003

Nugroho S, Sari D I, Zahra F, Rachmawati S, Maulana B S and Estiati A. (2021). Resistant performance of T10 Rojolele transgenic rice events harboring cry1B::cry1Aa fusion genes against the rice yellow stem borer Scirpophaga incertulas Wlk. IOP Conference Series: Earth and Environmental Science 762(1): 012067. https://doi.org/10.1088/1755-1315/762/1/012067

Nugroho S, Estiati A and Slamet-Loedin I H (2021). Development of yellow stem borer resistant rice varieties in Indonesia. In G T Gujar, Y A Trisyono and M Chen (Eds.), Genetically modified crops in asia pacific. Clayton, Australia: CSIRO Publishing, 245–254.

Oktavianti R, Nurdin J and Herwina H. (2017). Komunitas Collembola pada hutan konservasi dan perkebunan sawit di kawasan PT. Tidar Kerinci Agung (TKA), Sumatera Barat. Jurnal Biologi Universitas Andalas 5(1): 16–24.

Pielou E C. (1966). The measurement of diversity in different types of biological collections. Journal of Theoretical Biology 13: 131–144. https://doi.org/10.1016/0022-5193(66)90013-0

Prakash D, Verma S, Bhatia R and Tiwary B N. (2011). Risks and precautions of genetically modified organisms. International Scholarly Research Notices (ISRN) Ecology 2011: 1–13. https://doi.org/10.5402/2011/369573

Rahmawati S and Slamet-Loedin I H. (2006). Introduction of cryIB-cryIAa hybrid gene into rice (Oryza sativa) genom cv. Rojolele using agrobacterium-mediated transformation. Hayati Journal of Biosciences 13(1): 19–25. https://doi.org/10.1016/S1978-3019(16)30374-6

Settle W H and Whitten M J. (2000). The rule of small scale farmers in stengthening linkages between biodiversity and sustainable agriculture. Paper presented at the XXI International Congres of Entomology, Foz do Iguassu, Brazil, 20–26 August, 20–26.

Suhardjono Y R, Deharveng L and Bedos A. (2012). Biologi, ekologi, klasifikasi Collembola (ekor pegas). Bogor: Vagamedia.

Usyati N, Buchori D and Manuwoto S. (2009). Effectiveness of transgenic rice to the rice yellow stemborer Scirpophaga incertulas (Walker) (Lepidoptera: Crambidae). Jurnal Entomologi Indonesia 6(1): 30–41.

Visser S. (1985). Role of the soil invertebrates in determining the composition of soil microbial communities. In A H Fitter and D Atkinson (Eds.), Biological interaction in soil. Oxford, UK: Blackwell Scientific Publisher, 297–317.

Warino J, Widyastuti R, Rahayuningsih Suhardjono Y and Nugroho B. (2017). Keanekaragaman dan kelimpahan Collembola pada perkebunan kelapa sawit di Kecamatan Bajubang, Jambi. Jurnal Entomology Indonesia 14(2): 51–57. https://doi.org/10.5994/jei.14.2.51

Widrializa, Widyastuti R, Santosa D A and Djajakirana G. (2015). The diversity and abundance of springtail (Collembola) on forests and smallholder in Jambi. Journal of Tropical Soils 20(3): 173–180. https://doi.org/10.5400/jts.2015.20.3

Widyastuti R. (2005). Population dynamics of microarthropods (Oribatida and Collembola) in rainfed paddy field ecosystem in Pati, Central Java. Jurnal Tanah dan Lingkungan 7(1): 11–14. https://doi.org/10.29244/jitl.7.1.11-14

Woiwod I P and Magurran A E. (1990). Ecological diversity and its measurement. Biometrics 46(2): 547. https://doi.org/10.2307/2531473

Yaqoob A, Shahid A A, Samiullah T R, Rao A Q, Khan M A U, Tahir S, Mirza S A and Husnain T. (2016). Risk assessment of Bt crops on the non-target plant-associated insects and soil organisms. Journal of the Science of Food and Agriculture 96(8): 2613–2619. https://doi.org/10.1002/jsfa.7661