Abstract
Main conclusion
Domestication affected the abundances and diversity of maize root volatiles more than northward spread and modern breeding, and herbivore preference for roots was correlated with volatile diversity and herbivore resistance.
Abstract
Studies show that herbivore defenses in crops are mediated by domestication, spread, and breeding, among other human-driven processes. They also show that those processes affected chemical communication between crop plants and herbivores. We hypothesized that (i) preference of the herbivore (Diabrotica virgifera virgifera) larvae for embryonic roots of maize (Zea mays mays) would increase and (ii) root volatile diversity would decrease with the crop’s domestication, northward spread to present-day USA, and modern breeding. We used Balsas teosinte (Zea mays parviglumis), Mexican and USA landrace maizes, and US inbred maize lines to test these hypotheses. We found that herbivore preference and volatile diversity increased with maize domestication and northward spread but decreased with modern breeding. Additionally, we found that the abundances of single volatiles did not consistently increase or decrease with maize domestication, spread, and breeding; rather, volatiles grouped per their abundances were differentially affected by those processes, and domestication had the greatest effects. Altogether, our results suggested that: the herbivore’s preference for maize roots is correlated with volatile diversity and herbivore resistance; changes in abundances of individual volatiles are evident at the level of volatile groups; and maize domestication, but not spread and breeding, affected the abundances of some green leaf volatiles and sesquiterpenes/sesquiterpenoids. In part, we discussed our results in the context of herbivore defense evolution when resources for plant growth and defense vary across environments. We suggested that variability in relative abundance of volatiles may be associated with their local, functional relevance across wild and agricultural environments.
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Data will be made available upon reasonable request.
Abbreviations
- GLVs:
-
Green leaf volatiles
- WCR:
-
Western corn rootworm (Diabrotica virgifera virgifera)
- VOCs:
-
Volatile organic compounds
- Teosinte:
-
Balsas teosinte
- Mex landrace:
-
Mexican landrace maize
- US landrace:
-
US landrace maize
- US elite:
-
US inbred maize
- MT:
-
Monoterpene/monoterpenoid
- ST:
-
Sequiterpene/sesquiterpenoid
References
Abdi H (2007) The Bonferroni and Sidak corrections for multiple comparisons. In: Salkind N (ed) Encyclopedia of measurement and statistics. SAGE, Thousand Oaks, CA, USA
Agrawal AA, Conner JK, Rasmann S (2010) Tradeoffs and negative correlations in evolutionary ecology. In: Bell AM, Futuyma DJ, Eanes WF, Levinton JS (eds) Evolution since Darwin: the first 150 years. Oxford University, pp 243–268
Allmann S, Spathe A, Bisch-Knaden S, Kallenbach M, Reinecke A, Sachse S, Baldwin IT, Hansson BS (2013) Feeding-induced rearrangement of green leaf volatiles reduces moth oviposition. Elife 2:23. https://doi.org/10.7554/eLife.00421
Baldwin IT (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc Natl Acad Sci USA 95:8113–8118. https://doi.org/10.1073/pnas.95.14.8113
Bellota E, Medina RF, Bernal JS (2013) Physical leaf defenses – altered by Zea life-history evolution, domestication, and breeding – mediate oviposition preference of a specialist leafhopper. Ent Exp Appl 149:185–195. https://doi.org/10.1111/eea.12122
Benrey B, Callejas A, Rios L, Oyama K, Denno RF (1998) The effects of domestication of Brassica and Phaseolus on the interaction between phytophagous insects and parasitoids. Biol Control 11(2):130–140. https://doi.org/10.1006/bcon.1997.0590
Bernal JS, Medina RF (2018) Agriculture sows pests: how crop domestication, host shifts, and agricultural intensification can create insect pests from herbivores. Curr Opin Insect Sci 26:76–81. https://doi.org/10.1016/j.cois.2018.01.008
Bernal JS, Melancon JE, Zhu-Salzman K (2015) Clear advantages for fall armyworm larvae from feeding on maize relative to its ancestor Balsas teosinte may not be reflected in their mother’s host choice. Entomol Exp Appl 155:206–2017. https://doi.org/10.1111/eea.12299
Branson TF, Guss PL, Ortman EE (1969) Toxicity of sorghum roots to larvae of the western corn rootworm. Econ Entomol 62(6):1375–1378. https://doi.org/10.1093/jee/62.6.1375
Buckler ES, Stevens NM (2006) 4. Maize origins, domestication, and selection. In: Timothy M (ed) Darwin’s harvest. Columbia University Press, New York Chichester, West Sussex, pp 67–90
Carrasco D, Larsson MC, Anderson P (2015) Insect host plant selection in complex environments. Curr Opin Insect Sci 8:1–7. https://doi.org/10.1016/j.cois.2015.01.014
Carroll MJ, Schmelz EA, Teal PE (2008) The attraction of Spodoptera frugiperda neonates to cowpea seedlings is mediated by volatiles induced by conspecific herbivory and the elicitor inceptin. Chem Ecol 34(3):291–300. https://doi.org/10.1007/s10886-007-9414-y
Chen L, Luo J, Jin M, Yang N, Liu X et al (2022) Genome sequencing reveals evidence of adaptive variation in the genus Zea. Nat Genet 54(11):1736–1745. https://doi.org/10.1038/s41588-022-01184-y
Chen YH, Gols R, Benrey B (2015) Crop domestication and its impact on naturally selected trophic interactions. Annu Rev Entomol 60:35–58. https://doi.org/10.1146/annurev-ento-010814-020601
Chinchilla-Ramírez M, Borrego EJ, DeWitt TJ, Kolomiets MV, Bernal JS (2017) Maize seedling morphology and defence hormone profiles, but not herbivory tolerance, were mediated by domestication and modern breeding. Ann Appl Biol 170(3):315–332. https://doi.org/10.1111/aab.12331
Dávila-Flores AM, DeWitt TJ, Bernal JS (2013) Facilitated by nature and agriculture: performance of a specialist herbivore improves with host-plant life history evolution, domestication, and breeding. Oecologia 173(4):1425–1437. https://doi.org/10.1007/s00442-013-2728-2
de Lange ES, Balmer D, Mauch-Mani B, Turlings TCJ (2014) Insect and pathogen attack and resistance in maize and its wild ancestors, the teosintes. New Phytol 204(2):329–341. https://doi.org/10.1111/nph.13005
Degen T, Dillmann C, Marion-Poll F, Turlings TC (2004) High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol 135(4):1928–1938. https://doi.org/10.1104/pp.104.039891
Degenhardt J, Gershenzon J, Baldwin IT, Kessler A (2003) Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr Opin Biotech 14(2):169–176. https://doi.org/10.1016/s0958-1669(03)00025-9
Degenhardt J, Hiltpold IP, Köllner TG, Frey ML, Gierl A, Gershenzon A, Hibbard BE, Ellersieck MR, Turlings TCJ (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci USA 106(32):13213–13218
Ding Y, Huffaker A, Kollner TG, Weckwerth P, Robert CAM, Spencer JL, Lipka AE, Schmelz EA (2017) Selinene volatiles are essential precursors for maize defense promoting fungal pathogen resistance. Plant Physiol 175(3):1455–1468. https://doi.org/10.1104/pp.17.00879
Doebley J, Wendel JD, Smith JSC, Stuber CW, Goodman MM (1988) The origin of cornbelt maize: the isozyme evidence. Econ Bot 42(1):120–131. https://doi.org/10.1007/BF02859042
Duvick DN (2005) The contribution of breeding to yield advances in maize (Zea mays L.). Adv Agronomy 86:83–145. https://doi.org/10.1016/s0065-2113(05)86002-x.ISBN:9780120007844
Erb M (2018) Plant defenses against herbivory: closing the fitness gap. Trends Plant Sci 23(3):187–194. https://doi.org/10.1016/j.tplants.2017.11.005
Erb M, Balmer D, De Lange ES, Von Merey G, Planchamp C, Robert CA, Roder G, Sobhy I, Zwahlen C, Mauch-Mani B, Turlings TC (2011a) Synergies and trade-offs between insect and pathogen resistance in maize leaves and roots. Plant Cell Environ 34(7):1088–1103. https://doi.org/10.1111/j.1365-3040.2011.02307.x
Erb M, Kollner TG, Degenhardt J, Zwahlen C, Hibbard BE, Turlings TC (2011b) The role of abscisic acid and water stress in root herbivore-induced leaf resistance. New Phytol 189(1):308–320. https://doi.org/10.1111/j.1469-8137.2010.03450.x
Faiola C, Taipale D (2020) Impact of insect herbivory on plant stress volatile emissions from trees: a synthesis of quantitative measurements and recommendations for future research. Atmos Environ. https://doi.org/10.1016/j.aeaoa.2019.100060
Fontana A, Held M, Fantaye CA, Turlings TC, Degenhardt J, Gershenzon J (2011) Attractiveness of constitutive and herbivore-induced sesquiterpene blends of maize to the parasitic wasp Cotesia marginiventris (Cresson). Chem Ecol 37(6):582–591. https://doi.org/10.1007/s10886-011-9967-7
Fontes-Puebla AA, Bernal JS (2020) Resistance and tolerance to root herbivory in maize were mediated by domestication, spread, and breeding. Front Plant Sci 11:223. https://doi.org/10.3389/fpls.2020.00223
Fontes-Puebla AA, Borrego EJ, Kolomiets MV, Bernal JS (2021) Maize biochemistry in response to root herbivory was mediated by domestication, spread, and breeding. Planta 254(4):70. https://doi.org/10.1007/s00425-021-03720-2
Gaillard MDP, Glauser G, Robert CAM, Turlings TCJ (2018) Fine-tuning the “plant domestication-reduced defense” hypothesis: specialist vs generalist herbivores. New Phytol 217:355–366. https://doi.org/10.1111/nph.14757
Gouinguené S, Degen T, Turlings TCJ (2001) Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 11(1):9–16. https://doi.org/10.1007/PL00001832
Gouinguene SP, Turlings TCJ (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129(3):1296–1307. https://doi.org/10.1104/pp.001941
Gray ME, Sappington TW, Miller NJ, Moeser J, Bohn MO (2009) Adaptation and invasiveness of western corn rootworm: intensifying research on a worsening pest. Annu Rev Entomol 54:303–321. https://doi.org/10.1146/annurev.ento.54.110807.090434
Gripenberg S, Mayhew PJ, Parnell M, Roslin T (2010) A meta-analysis of preference-performance relationships in phytophagous insects. Ecol Lett 13(3):383–393. https://doi.org/10.1111/j.1461-0248.2009.01433.x
Grunseich JM, Thompson MN, Aguirre NM, Helms AM (2019) The role of plant-associated microbes in mediating host plant selection by insect herbivores. Plants 9(1):1–23. https://doi.org/10.3390/plants9010006
Grunseich JM, Thompson MN, Hay AA, Gorman Z, Kolomiets MV, Eubanks MD, Helms AM, Holeski L (2020) Risky roots and careful herbivores: sustained herbivory by a root-feeding herbivore attenuates indirect plant defences. Funct Ecol 34(9):1779–1789. https://doi.org/10.1111/1365-2435.13627
Hahn PG, Maron JL (2016) A framework for predicting intraspecific variation in plant defense. Trends Ecol Evol 31(8):646–656. https://doi.org/10.1016/j.tree.2016.05.007
Heil M (2014) Herbivore-induced plant volatiles: targets, perception and unanswered questions. New Phytol 204(2):297–306. https://doi.org/10.1111/nph.12977
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. The Quart Rev of Biol 63(3):283–335
Hernandez-Cumplido J, Giusti MM, Zhou Y, Kyryczenko-Roth V, Chen YH, Rodriguez-Saona C (2018) Testing the ‘plant domestication-reduced defense’ hypothesis in blueberries: the role of herbivore identity. Arthropod Plant Interact 12(4):483–493. https://doi.org/10.1007/s11829-018-9605-1
Hibbard BE, Bjostad LB (1988) Behavioral responses of Western corn rootworm larvae to volatile semiochemicals from corn seedlings. Chem Ecol 14(6):1523–1539. https://doi.org/10.1007/bf01012424
Hill RE (1975) Mating, oviposition patterns, fecundity and longevity of the Western corn rootworm. Econ Entomol 68(3):311–315. https://doi.org/10.1093/jee/68.3.311
Hiltpold I, Erb M, Robert CA, Turlings TC (2011) Systemic root signalling in a belowground, volatile-mediated tritrophic interaction. Plant Cell Environ 34(8):1267–1275. https://doi.org/10.1111/j.1365-3040.2011.02327.x
Hiltpold I, Turlings TC (2008) Belowground chemical signaling in maize: when simplicity rhymes with efficiency. J Chem Ecol 34(5):628–635. https://doi.org/10.1007/s10886-008-9467-6
Klimm FS, Weinhold A, Volf M (2020) Volatile production differs between oak leaves infested by leaf-miner Phyllonorycter harrisella (Lepidoptera: Gracillariidae) and galler Neuroterus quercusbaccarum (Hymenoptera: Cynipidae). Eur J Entomol 117:101–109. https://doi.org/10.14411/eje.2020.011
Köllner TG, Held M, Lenk C, Hiltpold I, Turlings TC, Gershenzon J, Degenhardt J (2008a) A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20(2):482–494. https://doi.org/10.1105/tpc.107.051672
Köllner TG, Schnee C, Gershenzon J, Degenhardt J (2004a) The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distributions. Phytochemistry 65(13):1895–1902. https://doi.org/10.1016/j.phytochem.2004.05.021
Köllner TG, Schnee C, Gershenzon J, Degenhardt J (2004b) The variability of sesquiterpenes emitted from two Zea mays cultivars is controlled by allelic variation of two terpene synthase genes encoding stereoselective multiple product enzymes. Plant Cell 16(5):1115–1131. https://doi.org/10.1105/tpc.019877
Köllner TG, Schnee C, Li S, Svatos A, Schneider B, Gershenzon J, Degenhardt J (2008b) Protonation of a neutral (S)-beta-bisabolene intermediate is involved in (S)-beta-macrocarpene formation by the maize sesquiterpene synthases TPS6 and TPS11. Biol Chem 283(30):20779–20788. https://doi.org/10.1074/jbc.M802682200
Kutka F (2011) Open-pollinated vs. hybrid maize cultivars. Sustainability 3(9):1531–1554. https://doi.org/10.3390/su3091531
Lombaert E, Ciosi M, Miller NJ, Sappington TW, Blin A, Guillemaud T (2017) Colonization history of the western corn rootworm (Diabrotica virgifera virgifera) in North America: insights from random forest ABC using microsatellite data. Biol Invasions 20:665–677. https://doi.org/10.1007/s10530-017-1566-2
Macfadyen S, Bohan DA (2010) Crop domestication and the disruption of species interactions. Basic Appl Ecol 11(2):116–125. https://doi.org/10.1016/j.baae.2009.11.008
Machado RAR, Theepan V, Robert CAM, Zust T, Hu L, Su Q, Schimmel BCJ, Erb M (2021) The plant metabolome guides fitness-relevant foraging decisions of a specialist herbivore. PLoS Biol 19(2):e3001114. https://doi.org/10.1371/journal.pbio.3001114
Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez GJ, Buckler E, Doebley J (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99(9):6080–6084. https://doi.org/10.1073/pnas.052125199
Meinke LJ, Sappington TW, Onstad DW, Guillemaud T, Miller NJ, Komáromi J, Levay N, Furlan L, Kiss J, Toth F (2009) Western corn rootworm (Diabrotica virgifera virgifera LeConte) population dynamics. Agric for Entomol 11:29–46. https://doi.org/10.1111/j.1461-9563.2008.00419.x
Morris EK, Caruso T, Buscot F, Fischer M, Hancock C et al (2014) Choosing and using diversity indices: insights for ecological applications from the German biodiversity exploratories. Ecol Evol 4(18):3514–3524. https://doi.org/10.1002/ece3.1155
Murphy SM (2004) Enemy-free space maintains swallowtail butterfly host-shift. Proc Natl Acad Sci USA 101(52):18048–18052. https://doi.org/10.1073/pnas.0406490102
Paddock KJ, Robert CAM, Erb M, Hibbard BE (2021) Western corn rootworm, plant and microbe interactions: a review and prospects for new management tools. InSects 12(2):171. https://doi.org/10.3390/insects12020171
Perkins JH (1982) Insects, experts and the insecticide crisis: the quest for new pest management strategies. Plenum Press, New York
Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TC (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737. https://doi.org/10.1038/nature03451
Reisenman CE, Riffell JA, Bernays EA, Hildebrand JG (2010) Antagonistic effects of floral scent in an insect-plant interaction. Proc Biol Sci 277(1692):2371–2379. https://doi.org/10.1098/rspb.2010.0163
Robert CA, Veyrat N, Glauser G, Marti G, Doyen GR, Villard N, Gaillard MD, Köllner TG, Giron D, Body M, Babst BA, Ferrieri RA, Turlings TC, Erb M (2012) A specialist root herbivore exploits defensive metabolites to locate nutritious tissues. Ecol Lett 15(1):55–64. https://doi.org/10.1111/j.1461-0248.2011.01708.x
Rodriguez-Saona C, Vorsa N, Singh AP, Johnson-Cicalese J, Szendrei Z, Mescher MC, Frost CJ (2011) Tracing the history of plant traits under domestication in cranberries: potential consequences on anti-herbivore defences. Exp Bot 62(8):2633–2644. https://doi.org/10.1093/jxb/erq466
Rojas JC, Kolomiets MV, Bernal JS (2018) Nonsensical choices? Fall armyworm moths choose seemingly best or worst hosts for their larvae, but neonate larvae make their own choices. PLoS ONE 13(5):e0197628. https://doi.org/10.1371/journal.pone.0197628
Ross-Ibarra J, Piperno D (2020) Maize moving. figshare. https://doi.org/10.6084/m9.figshare.12781307.v1
Rowen E, Kaplan I (2016) Eco-evolutionary factors drive induced plant volatiles: a meta-analysis. New Phytol 210(1):284–294. https://doi.org/10.1111/nph.13804
SAS Institute Inc. (2018) JMP Pro 14.0.0 ed. Cary, NC
Solis-Montero V, Martinez-Nataren DA, Parra-Tabla V, Ibarra-Cerdena C, Munguia-Rosas MA (2020) Herbivory and anti-herbivore defences in wild and cultivated Cnidoscolus aconitifolius: disentangling domestication and environmental effects. AoB Plants 12(3):plaa023. https://doi.org/10.1093/aobpla/plaa023
Strnad SP, Dunn PE (1990) Host search behavior of neonate western corn rootworm (Diabrotica virgifera virgifera). Insect Physiol 36(3):201–205. https://doi.org/10.1016/0022-1910(90)90123-W
Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12(4):479–485. https://doi.org/10.1016/j.pbi.2009.04.001
van Heerwaarden J, Hufford MB, Ross-Ibarra J (2012) Historical genomics of North American maize. Proc Natl Acad Sci USA 109(31):12420–12425. https://doi.org/10.1073/pnas.1209275109
Wetzel WC, Whitehead SR (2020) The many dimensions of phytochemical diversity: linking theory to practice. Ecol Lett 23(1):16–32. https://doi.org/10.1111/ele.13422
Zaiontz C (2020) Real Statistics Using Excel. www.real-statistics.com
Zalucki MP, Clarke AR, Malcolm SB (2002) Ecology and behavior of first instar larval lepidoptera. Annu Rev Entomol 47:361–393. https://doi.org/10.1146/annurev.ento.47.091201.145220
Zust T, Agrawal AA (2017) Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annu Rev Plant Biol 68:513–534. https://doi.org/10.1146/annurev-arplant-042916-040856
Acknowledgements
We thank Chad Nielson (USDA ARS, Brookings, SD, United States) for providing western corn rootworm eggs, and Mark Millard (USDA NPGS, Ames, IA, United States) for providing Mo17, and Mexican and US maize landrace seed. R. F. Medina and K. Zhu-Salzman (both Texas A&M University, College Station) provided advice on earlier versions of the manuscript. Two anonymous reviewers provided valuable advice which helped us to meaningfully improve the manuscript.
Funding
This study was supported in part by funding from Consejo Nacional de Ciencia y Tecnología (CONACyT) and Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias (INIFAP), both Mexico, to AAF-P (CONACyT scholarship #382690); Texas A&M University-CONACyT [Characterization of Resistance to Root- And Foliage-Feeding Insects in Maize Breeding Lines, Landraces, and Wild Ancestors, Project 2014–024(S)] and the United States Department of Agriculture (USDA) Hatch (TEX07234) to JSB, and; USDA-National Institute of Food and Agriculture (NIFA) to MVK and JSB [Lipid-Mediated Signaling Govern Maize Resistance To Below- and Above-Ground Insect Herbivores, Project USDA-NIFA (2021-67013-33568)].
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Correlation between volatiles and WCR host preference as measured in assay Preference for Zea plant types relative to a non-host (see Fig. 4a) (PNG 128 KB)
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Output of random forest analyses showing volatile compounds that were most relevant to explaining variation among plant types (PNG 101 KB)
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Bernal, J.S., Helms, A.M., Fontes-Puebla, A.A. et al. Root volatile profiles and herbivore preference are mediated by maize domestication, geographic spread, and modern breeding. Planta 257, 24 (2023). https://doi.org/10.1007/s00425-022-04057-0
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DOI: https://doi.org/10.1007/s00425-022-04057-0