Abstract
Climate variability has major implications for agriculture due to the increase in the frequency and intensity of simultaneous abiotic, namely water-stress, and biotic stresses to crops. Plant water-stress alone harms crops but also can attract outbreaks of herbivores with varied host specialization, and plants succumb to further yield losses dealing with multiple stressors. Host plant resistance provides a route to lessen yield losses from herbivory; however, our knowledge of the interactions between water-stress and pest resistance is limited, especially for mite herbivores of maize including the generalist two-spotted spider mite (Tetranychus urticae, TSM) and the specialist Banks grass mite (Oligonychus pratensis, BGM). We conducted parallel greenhouse and field experiments whereby a susceptible line (B73) and two TSM-resistant lines (B75 and B96) were subjected to either optimal irrigation or water-stress [50–60% and 5–10% volumetric water content (VWC), and 25–32% and 10–15% VWC, in the greenhouse and field, respectively] to test whether pest-resistant lines maintain their resistance when exposed to water-stress. We found that under optimal irrigation, TSM and BGM populations increased readily on B73, while B75 and B96 were largely resistant to the TSM but not BGM. While plant water-stress increased the susceptibility of B73 to both mite species, water-stress did not disrupt initial resistance levels of B75 and B96 maize for either mite species. Elevated protease activity was found in B75 and B96 and may contribute to maize resistance. Our findings that B75 and B96 are highly resistant to the TSM, and maintain resistance to both mite species with water-stress, highlight the importance of including the nuances of multiple stressors within the framework of host plant resistance.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The datasets generated during and/or analyzed during the current study are available in the DRYAD repository.https://doi.org/10.5061/dryad.mgqnk992g
References
Archer TL (1987) Techniques for screening maize for resistance to mites, In: Proceedings of the international symposium on methodologies for developing host plant resistance to maize insects. 187–183.
Archer TL, Bynum ED (1993) Yield loss to corn from feeding by the Banks grass mite and two-spotted spider mite (Acari: Tetranychidae). Exp Appl Acarol. https://doi.org/10.1007/BF02328066
Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2012.02.006
Arnaiz A, Talavera-Mateo L, Gonzalez-Melendi P et al (2018) Arabidopsis kunitz trypsin inhibitors in defense against spider mites. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00986
Barry D, Alfaro D, Darrah LL (1994) Relation of European corn borer (Lepidoptera: Pyralidae) leaf-feeding resistance and DIMBOA content in maize. Environ Entomol. https://doi.org/10.1093/ee/23.1.177
Bing JW, Guthrie WD, Dicke FF, Obryckp JJ (1990) Relation of corn leaf aphid (Homoptera: Aphididae) colonization to DIMBOA content in maize inbred lines. J Econ Entomol. https://doi.org/10.1093/jee/83.4.1626
Bui H, Greenhalgh R, Gill GS, Ji M, Kurlovs AH, Ronnow C, Lee S, Ramirez RA, Clark RM (2021) Maize inbred line B96 is the source of large-effect loci for resistance to generalist but not specialist spider mites. Front Plant Sci. https://doi.org/10.3389/fpls.2021.693088
Bui H, Greenhalgh R, Ruckert A, Gill GS, Lee S, Ramirez RA, Clark RM (2018) Generalist and specialist mite herbivores induce similar defense responses in maize and barley but differ in susceptibility to benzoxazinoids. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01222
Bynum ED, Xu W, Archer TL (2004) Diallel analysis of spider mite resistant maize inbred lines and F 1 crosses. Crop Sci. https://doi.org/10.2135/cropsci2004.1535
Cao HH, Pan MZ, Liu HR, Wang SH, Liu TX (2015) Antibiosis and tolerance but not antixenosis to the grain aphid, Sitobion avenae (Hemiptera: Aphididae), are essential mechanisms of resistance in a wheat cultivar. Bull Entomol Res. https://doi.org/10.1017/S0007485315000322
Cipollini D, Enright S, Traw MB, Bergelson J (2004) Salicylic acid inhibits jasmonic acid-induced resistance of Arabidopsis thaliana to Spodoptera exigua. Mol Ecol. https://doi.org/10.1111/j.1365-294X.2004.02161.x
English-Loeb G, Stout MJ, Duffey SS (1997) Drought stress in tomatoes: Changes in plant chemistry and potential nonlinear consequences for insect herbivores. Oikos. https://doi.org/10.2307/3546888
English-Loeb GM (1990) Plant drought stress and outbreaks of spider mites: a field test. Ecology. https://doi.org/10.2307/1938277
Fritter AH, Hay RKM (2012) Environmental physiology of plants. Academic press. https://www.elsevier.com/books/environmental-physiology-of-plants/fitter/978-0-08-054981-1
Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci. https://doi.org/10.3390/ijms140510242
Gill GS, Bui H, Clark RM, Ramirez RA (2020) Varying responses to combined water-stress and herbivory in maize for spider mite species that differ in host specialization. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2020.104131
Glas JJ, Alba JM, Simoni S et al (2014) Defense suppression benefits herbivores that have a monopoly on their feeding site but can backfire within natural communities. BMC Biol. https://doi.org/10.1186/s12915-014-0098-9
Grbić M, Van Leeuwen T, Clark RM et al (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature. https://doi.org/10.1038/nature10640
Grinnan R, Carter TE, Johnson MTJ (2013) Effects of drought, temperature, herbivory, and genotype on plant-insect interactions in soybean (Glycine max). Arthropod-Plant Interact. https://doi.org/10.1007/s11829-012-9234-z
Isoda A, Shahenshah, (2010) Effects of water stress on leaf temperature and chlorophyll fluorescence parameters in cotton and peanut. Plant Product Sci. https://doi.org/10.1626/pps.13.269
Kamali K, Dicke FF, Guthrie WD (1989) Resistance-susceptibility of maize genotypes to artificial infestations by twospotted spider mites. Crop Sci. https://doi.org/10.2135/cropsci1989.0011183X002900040020x
Kramer PJ (1983) Water relations of plants. Cell Water Relations. https://doi.org/10.1016/B978-0-12-425040-6.50005-9
Mander L, Liu HW (2010) Comprehensive natural products II: chemistry and biology. https://doi.org/10.1016/C2009-1-28362-6
Maxmen A (2013) Crop pests: Under attack. Nature. https://doi.org/10.1038/501S15a
Migeon A, Nouguier E, Dorkeld F (2010) Spider Mites Web: A comprehensive database for the Tetranychidae. In: Sabelis MW, Bruin J (eds) Trends in acarology. Springer Netherlands, Dordrecht, pp 557–560. https://doi.org/10.1007/978-90-481-9837-5_96
Minibayeva F, Beckett RP, Kranner I (2015) Roles of apoplastic peroxidases in plant response to wounding. Phytochemistry. https://doi.org/10.1016/j.phytochem.2014.06.008
Oerke EC (2006) Crop losses to pests. J Agric Sci. https://doi.org/10.1017/S0021859605005708
Owens JC, Ward CR., Teetes GL (1976) Current status of spider mites in corn and sorghum, In: Proceeding. 31st annual corn and sorghum conference. Chicago, IL, USA,38–64.
Portwood JL et al (2019) MaizeGDB 2018: the maize multi-genome genetics and genomics database. Nucleic Acids Res 47:D1146–D1154. https://doi.org/10.1093/nar/gky1046
Romay MC et al (2013) Comprehensive genotyping of the USA national maize inbred seed bank. Genome Biol. https://doi.org/10.1186/gb-2013-14-6-r55
Ruckert A, Allen LN, Ramirez RA (2018) Combinations of plant water-stress and neonicotinoids can lead to secondary outbreaks of Banks grass mite (Oligonychus pratensis Banks). PLoS ONE. https://doi.org/10.1371/journal.pone.0191536
Ruckert A, Golec JR, Barnes CL, Ramirez RA (2021) Banks grass mite suppression may add to the benefit of drought-tolerant corn hybrids exposed to water-stress. Econ Entomol. https://doi.org/10.1093/jee/toaa269
Santamaria ME, Diaz I, Martinez M (2018) Dehydration stress contributes to the enhancement of plant defense response and mite performance on barley. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00458
Schnable PS et al (2009) The B73 maize genome: Complexity, diversity, and dynamics. Science. https://doi.org/10.1126/science.1178534
Sharma HC, Mukuru SZ, Manyasa E, Were JW (1999) Breakdown of resistance to sorghum midge, Stenodiplosis sorghicola. Euphytica. https://doi.org/10.1023/A:1003724217514
Suzuki H, Dowd PF, Johnson ET, Hum-Musser SM, Musser RO (2012) Effects of elevated peroxidase levels and corn earworm feeding on gene expression in tomato. J Chem Ecol. https://doi.org/10.1007/s10886-012-0205-8
Tadmor Y, Lewinsohn E, Abo-Moch F, Bar-Zur A, Mansour F (1999) Antibiosis of maize inbred lines to the carmine spider mite Tetranychus cinnabarinus. Phytoparasitica. https://doi.org/10.1007/BF02980725
Thipyapong P, Melkonian J, Wolfe DW, Steffens JC (2004) Suppression of polyphenol oxidases increases stress tolerance in tomato. Plant Sci. https://doi.org/10.1016/j.plantsci.2004.04.008
Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: A review. Insect Biochem Mol Biol. https://doi.org/10.1016/j.ibmb.2010.05.008
Verdugo JA, Francis F, Ramírez, CC, (2016) A review on the complexity of insect-plant interactions under varying levels of resources and host resistance: the case of Myzus persicae-Prunus persica. Biotechnol Agron Soc Environ. https://doi.org/10.25518/1780-4507.13218
Verdugo JA, Sauge MH, Lacroze JP, Francis F, Ramirez CC (2015) Drought-stress and plant resistance affect herbivore performance and proteome: the case of the green peach aphid Myzus persicae (Hemiptera: Aphididae). Physiol Entomol. https://doi.org/10.1111/phen.12111
Willmot DB, Hibbard BE, Darrah LL et al (2009) Effect of environment on resistance to the European corn borer (Lepidoptera: Crambidae) in maize. J Econ Entomol. https://doi.org/10.1603/0022-0493-97.5.1745
Wouters FC, Blanchette B, Gershenzon J, Vassão DG (2016) Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores. Phytochem Rev. https://doi.org/10.1007/s11101-016-9481-1
Ximénez-Embún MG, Castañera P, Ortego F (2017) Drought stress in tomato increases the performance of adapted and non-adapted strains of Tetranychus urticae. J Insect Physiol. https://doi.org/10.1016/j.jinsphys.2016.10.015
Ximénez-Embún MG, González-Guzmán M, Arbona V, Gómez-Cadenas A, Ortego F, Castañera P (2018) Plant-mediated effects of water deficit on the performance of Tetranychus evansi on tomato drought-adapted accessions. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01490
Zheng L, McMullen MD, Bauer E, Schon C-C, Gierl A, Frey M (2015) Prolonged expression of the BX1 signature enzyme is associated with a recombination hotspot in the benzoxazinoid gene cluster in Zea mays. J Exp Bot. https://doi.org/10.1093/jxb/erv192
Acknowledgements
We thank S. Vivas, L. Hendricksen, S. Gonzalez and B. Steadman for assisting in the experimental setup, sample collection and processing, and protein assays. This study was supported by the USA National Science Foundation (NSF) Plant Genome Research Program award 1444449 to RMC and RAR.
Funding
This research was supported by the USA National Science Foundation (NSF) Plant Genome Research Program award 1444449 to RC and RR.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests
The authors have no relevant financial or non-financial interests to disclose.
Ethical approval
Not applicable.
Additional information
Communicated by Cesar Rodriguez-Saona
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gill, G.S., Bui, H., Clark, R.M. et al. Spider mite resistant maize lines, B75 and B96, maintain resistance under water-stress. J Pest Sci 96, 1117–1132 (2023). https://doi.org/10.1007/s10340-022-01584-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-022-01584-3