Ongoing ecological and evolutionary consequences by the presence of transgenes in a wild cotton population.

Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101563288 Publication Model: Electronic Cited Medium: Internet ISSN: 2045-2322 (Electronic) Linking ISSN: 20452322 NLM ISO Abbreviation: Sci Rep Subsets: MEDLINE

Original Publication: London : Nature Publishing Group, copyright 2011-

Ecology* ; Evolution, Molecular* ; Genes, Plant* ; Transgenes*; Gossypium/*genetics ; Plants, Genetically Modified/*genetics; Animals ; Ants/physiology ; Gene Expression Regulation, Plant ; Gene Flow ; Gossypium/physiology ; Herbivory ; Mexico ; Plant Nectar

After 25 years of genetically modified cotton cultivation in Mexico, gene flow between transgenic individuals and their wild relatives represents an opportunity for analysing the impacts of the presence of novel genes in ecological and evolutionary processes in natural conditions. We show comprehensive empirical evidence on the physiological, metabolic, and ecological effects of transgene introgression in wild cotton, Gossypium hirsutum. We report that the expression of both the cry and cp4-epsps genes in wild cotton under natural conditions altered extrafloral nectar inducibility and thus, its association with different ant species: the dominance of the defensive species Camponotus planatus in Bt plants, the presence of cp4-epsps without defence role of Monomorium ebeninum ants, and of the invasive species Paratrechina longicornis in wild plants without transgenes. Moreover, we found an increase in herbivore damage to cp4-epsps plants. Our results reveal the influence of transgene expression on native ecological interactions. These findings can be useful in the design of risk assessment methodologies for genetically modified organisms and the in situ conservation of G. hirsutum metapopulations.

Ellstrand, N. C., Prentice, H. C. & Hancock, J. F. Gene flow and introgression from domesticated plants into their wild relatives. Annu. Rev. Ecol. Syst. 30, 539–563 (1999). (PMID: 10.1146/annurev.ecolsys.30.1.539)
Wegier, A. et al. Recent long-distance transgene flow into wild populations conforms to historical patterns of gene flow in cotton (Gossypiumhirsutum) at its centre of origin. Mol. Ecol. 20, 4182–4194 (2011). (PMID: 2189962110.1111/j.1365-294X.2011.05258.x)
Hernández-Terán, A. et al. In vitro performance in cotton plants with different genetic backgrounds: The case of Gossypiumhirsutum in Mexico, and its implications for germplasm conservation. PeerJ 7, 1–18 (2019). (PMID: 10.7717/peerj.7017)
Snow, A. A. et al. A Bt transgene reduces herbivory and enhances fecundity in wild sunflowers. Ecol. Appl. 13, 279–286 (2003). (PMID: 10.1890/1051-0761(2003)013[0279:ABTRHA]2.0.CO;2)
Yang, X. et al. Genetically engineered rice endogenous 5-enolpyruvoylshikimate-3-phosphate synthase (epsps) transgene alters phenology and fitness of crop-wild hybrid offspring. Sci. Rep. 7, 1–12 (2017).
Manshardt, R., Bishaw, D., Pitz, K. & Stewart, C. N. Gene flow from commercial transgenic papaya fields into feral populations in Hawaii. Acta Hortic. 1124, 33–40 (2016). (PMID: 10.17660/ActaHortic.2016.1124.5)
Ellstrand, N. C. “Born to run”? Not necessarily: Species and trait bias in persistent free-living transgenic plants. Front. Bioeng. Biotechnol. 6, 1–10 (2018). (PMID: 10.3389/fbioe.2018.00088)
Elmore, R. W. et al. Glyphosate-resistant soybean cultivar yields compared with sister lines. Agron. J. 93, 408 (2001). (PMID: 10.2134/agronj2001.932408x)
Zhao, J. Z. et al. Transgenic plants expressing two Bacillusthuringiensis toxins delay insect resistance evolution. Nat. Biotechnol. 21, 1493–1497 (2003). (PMID: 1460836310.1038/nbt907)
Halpin, C. Gene stacking in transgenic plants—The challenge for 21st century plant biotechnology. Plant Biotechnol. J. 3, 141–155 (2005). (PMID: 1717361510.1111/j.1467-7652.2004.00113.x)
Feng, Y. J., Wang, J. W. & Luo, S. M. Effects of exogenous jasmonic acid on concentrations of direct-defense chemicals and expression of related genes in Bt (Bacillusthuringiensis) corn (Zeamays). Agric. Sci. China 6, 1456–1462 (2007). (PMID: 10.1016/S1671-2927(08)60008-5)
Torres, J. B., Ruberson, J. R. & Whitehouse, M. Transgenic Cotton for Sustainable Pest Management: A Review 15–53 (Springer, Dordrecht, 2009). https://doi.org/10.1007/978-1-4020-9654-9_4 . (PMID: 10.1007/978-1-4020-9654-9_4)
Rauschen, S., Schultheis, E., Pagel-Wieder, S., Schuphan, I. & Eber, S. Impact of Bt-corn MON88017 in comparison to three conventional lines on Trigonotyluscaelestialium (Kirkaldy) (Heteroptera: Miridae) field densities. Transgenic Res. 18, 203–214 (2009). (PMID: 1866833610.1007/s11248-008-9207-2)
Chen, Y. H., Shapiro, L. R., Benrey, B. & Cibrián-Jaramillo, A. Back to the origin: In situ studies are needed to understand selection during crop diversification. Front. Ecol. Evol. 5, 1–8 (2017). (PMID: 10.3389/fevo.2017.00125)
Strapasson, P., Pinto-Zevallos, D. M. & Zarbin, P. H. G. Soybean (Glycine max) plants genetically modified to express resistance to glyphosate: Can they modify airborne signals in tritrophic interactions?. Chemoecology 26, 7–14 (2016). (PMID: 10.1007/s00049-015-0202-9)
Erb, M. Volatiles as inducers and suppressors of plant defense and immunity—Origins, specificity, perception and signaling. Curr. Opin. Plant Biol. 44, 117–121 (2018). (PMID: 2967413010.1016/j.pbi.2018.03.008)
Kolseth, A. K. et al. Influence of genetically modified organisms on agro-ecosystem processes. Agric. Ecosyst. Environ. 214, 96–106 (2015). (PMID: 10.1016/j.agee.2015.08.021)
Ckers, F. L. W. & Bonifay, C. How to be sweet? Extrafloral nectar allocation by Gossypiumhirsutum fits optimal defense theory predictions. Spec. Featur. Ecol. 85, 1512–1518 (2004).
Rudgers, J. A., Strauss, S. Y. & Wendel, J. F. Trade-offs among anti-herbivore resistance traits: insights from Gossypieae (Malvaceae). Am. J. Bot. 91, 871–880 (2004). (PMID: 2165344310.3732/ajb.91.6.871)
Rudgers, J. A., Hodgen, J. G. & White, J. W. Behavioral mechanisms underlie an ant–plant mutualism. Oecologia 135, 51–59 (2003). (PMID: 1264710310.1007/s00442-002-1168-1)
Williams, L., Rodriguez-Saona, C. & del Conte, S. C. C. Methyl jasmonate induction of cotton: A field test of the ‘attract and reward’ strategy of conservation biological control. AoB Plants 9, 1–15 (2017). (PMID: 10.1093/aobpla/plx032)
Ramos-Zapata, J., Parra-Tabla, V., Leirana-Alcocer, J., González-Moreno, A. & Chiappa-Carrara, X. Ecología Funcional de la Reserva de la Biósfera de Ría Lagartos (2017).
Heil, M. Induction of two indirect defences benefits Lima bean (Phaseoluslunatus, Fabaceae) in nature. J. Ecol. 92, 527–536 (2004). (PMID: 10.1111/j.0022-0477.2004.00890.x)
Mooney, K. A. & Agrawal, A. A. Plant genotype shapes ant–aphid interactions: Implications for community structure and indirect plant defense. Am. Nat. 171, E195–E205 (2008). (PMID: 1841955110.1086/587758)
Hernandez-Cumplido, J., Forter, B., Moreira, X., Heil, M. & Benrey, B. Induced floral and extrafloral nectar production affect ant–pollinator interactions and plant fitness. Biotropica 48, 342–348 (2016). (PMID: 10.1111/btp.12283)
Machado, B. B. et al. BioLeaf: A professional mobile application to measure foliar damage caused by insect herbivory. Comput. Electron. Agric. 129, 44–55 (2016). (PMID: 10.1016/j.compag.2016.09.007)
Lindén, A. & Mäntyniemi, S. Using the negative binomial distribution to model overdispersion in ecological count data. Ecology 92, 1414–1421 (2011). (PMID: 2187061510.1890/10-1831.1)
Wang, L. & Wu, J. The essential role of jasmonic acid in plant-herbivore interactions—Using the wild tobacco Nicotianaattenuata as a model. J. Genet. Genomics 40, 597–606 (2013). (PMID: 2437786610.1016/j.jgg.2013.10.001)
Park, S. H., Scheffler, J., Scheffler, B., Cantrell, C. L. & Pauli, C. S. Chemical defense responses of upland cotton, Gossypiumhirsutum L. to physical wounding. Plant Direct 3, 1–15 (2019). (PMID: 10.1002/pld3.141)
Hagenbucher, S., Eisenring, M., Meissle, M. & Romeis, J. Interaction of transgenic and natural insect resistance mechanisms against Spodopteralittoralis in cotton. Pest Manag. Sci. 73, 1670–1678 (2017). (PMID: 2801906310.1002/ps.4510)
Zhang, P. et al. Suppression of jasmonic acid-dependent defense in cotton plant by the mealybug Phenacoccussolenopsis. PLoS ONE 6, e22378 (2011). (PMID: 21818315314489310.1371/journal.pone.0022378)
Kunkel, B. N. & Brooks, D. M. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5, 325–331 (2002). (PMID: 1217996610.1016/S1369-5266(02)00275-3)
Thaler, J. S., Humphrey, P. T. & Whiteman, N. K. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci. 17, 260–270 (2012). (PMID: 2249845010.1016/j.tplants.2012.02.010)
Verberne, M. C., Verpoorte, R., Bol, J. F., Mercado-Blanco, J. & Linthorst, H. J. M. Overproduction of salicylic acid in plants by bacterial transgenes enhances pathogen resistance. Nat. Biotechnol. 18, 779–783 (2000). (PMID: 1088884910.1038/77347)
Dempsey, D. A., Vlot, A. C., Wildermuth, M. C. & Klessig, D. F. Salicylic acid biosynthesis and metabolism. Arab. B. 9, e0156 (2011). (PMID: 10.1199/tab.0156)
Wäckers, F. L. & Wunderlin, R. Induction of cotton extrafloral nectar production in response to herbivory does not require a herbivore-specific elicitor. in Proceedings of the 10th International Symposium on Insect-Plant Relationships 149–154 (Springer Netherlands, 1999). https://doi.org/10.1007/978-94-017-1890-5_18 .
Yang, F. et al. Analysis of key genes of jasmonic acid mediated signal pathway for defense against insect damages by comparative transcriptome sequencing. Sci. Rep. 5, 16500 (2015). (PMID: 26560755464235110.1038/srep16500)
Chu, B. et al. Genetic regulation of defence responses in cotton to insect herbivores. AoB Plants 9, plx048 (2017). (PMID: 10.1093/aobpla/plx048)
Heil, M. Nectar: Generation, regulation and ecological functions. Trends Plant Sci. 16, 191–200 (2011). (PMID: 2134571510.1016/j.tplants.2011.01.003)
Rico-Gray, V. & Oliveira, P. S. The Ecology and Evolution of Ant–Plant Interactions (University of Chicago Press, Chicago, 2013). https://doi.org/10.7208/chicago/9780226713540.001.0001 . (PMID: 10.7208/chicago/9780226713540.001.0001)
Pacelhe, F. T., Costa, F. V., Neves, F. S., Bronstein, J. & Mello, M. A. R. Nectar quality affects ant aggressiveness and biotic defense provided to plants. Biotropica 51, 196–204 (2019). (PMID: 10.1111/btp.12625)
Oliveira, P. S., Rico-Gray, V., Díaz-Castelazo, C. & Castillo-Guevara, C. Interaction between ants, extrafloral nectaries and insect herbivores in Neotropical coastal sand dunes: Herbivore deterrence by visiting ants increases fruit set in Opuntiastricta (Cactaceae). Funct. Ecol. 13, 623–631 (1999). (PMID: 10.1046/j.1365-2435.1999.00360.x)
Koptur, S., William, P. & Olive, Z. Ants and plants with extrafloral nectaries in fire successional habitats on Andros (Bahamas). Fla. Entomol. 93, 89–99 (2010). (PMID: 10.1653/024.093.0112)
Cuautle, M., Rico-Gray, V. & Diaz-Castelazo, C. Effects of ant behaviour and presence of extrafloral nectaries on seed dispersal of the Neotropical myrmecochore Turneraulmifolia L. (Turneraceae). Biol. J. Linn. Soc. 86, 67–77 (2005). (PMID: 10.1111/j.1095-8312.2005.00525.x)
Rico-Gray, V. & Thien, T. B. Ant-mealybug interaction decreases reproductive fitness of Schomburgkiatibicinis (Orchidaceae) in Mexico. J. Trop. Ecol. 5, 109–112 (1989). (PMID: 10.1017/S0266467400003266)
Raine, N. E., Gammans, N., Macfadyen, I. J., Scrivner, G. K. & Stone, G. N. Guards and thieves: Antagonistic interactions between two ant species coexisting on the same ant–plant. Ecol. Entomol. 29, 345–352 (2004). (PMID: 10.1111/j.0307-6946.2004.00608.x)
Villamil, N., Boege, K. & Stone, G. N. Testing the distraction hypothesis: Do extrafloral nectaries reduce ant–pollinator conflict?. J. Ecol. 107, 1377–1391 (2019). (PMID: 31217634655932110.1111/1365-2745.13135)
Rico-Gray, V. & Thien, L. B. Effect of different ant species on reproductive fitness of Schomburgkiatibicinis (Orchidaceae). Oecologia 81, 487–489 (1989). (PMID: 2831264110.1007/BF00378956)
Diaz-Castelazo, C., Rico-Gray, V., Oliveira, P. S. & Cuautle, M. Extrafloral nectary-mediated ant–plant interactions in the coastal vegetation of Veracruz, Mexico: Richness, occurrence, seasonality, and ant foraging patterns. Ecoscience 11, 472–481 (2004). (PMID: 10.1080/11956860.2004.11682857)
Author, M., Rudgers, J. A. & Rudgers, J. A. Enemies of herbivores can shape plant traits: Selection in a facultative ant–plant. Source Ecol. Ecol. 85, 192–205 (2004).
Quijano-Medina, T., Covelo, F., Moreira, X. & Abdala-Roberts, L. Compensation to simulated insect leaf herbivory in wild cotton (Gossypiumhirsutum): Responses to multiple levels of damage and associated traits. Plant Biol. 21, 805–812 (2019). (PMID: 3105086310.1111/plb.13002)
Lang, A. & Otto, M. A synthesis of laboratory and field studies on the effects of transgenic Bacillusthuringiensis (Bt) maize on non-target Lepidoptera. Entomol. Exp. Appl. 135, 121–134 (2010). (PMID: 10.1111/j.1570-7458.2010.00981.x)
Schmidt, J. E. U., Braun, C. U., Whitehouse, L. P. & Hilbeck, A. Effects of activated Bt transgene products (Cry1Ab, Cry3Bb) on immature stages of the ladybird Adaliabipunctata in laboratory ecotoxicity testing. Arch. Environ. Contam. Toxicol. 56, 221–228 (2009). (PMID: 1871250110.1007/s00244-008-9191-9)
Romeis, J., Meissle, M. & Bigler, F. Transgenic crops expressing Bacillusthuringiensis toxins and biological control. Nat. Biotechnol. 24, 63–71 (2006). (PMID: 1640439910.1038/nbt1180)
Yu, H., Romeis, J., Li, Y., Li, X. & Wu, K. Acquisition of Cry1Ac protein by non-target arthropods in Bt soybean fields. PLoS ONE 9, e103973 (2014). (PMID: 25110881412881810.1371/journal.pone.0103973)

0 (Plant Nectar)

Date Created: 20210122 Date Completed: 20211006 Latest Revision: 20230127

20231215

PMC7820435

10.1038/s41598-021-81567-z

33479296