Abstract
White fringetree is a host for the invasive emerald ash borer (EAB) but is of lower quality than the related and highly susceptible black ash. Field observations suggest that host trees grown in full sun are more resistant to EAB than those in shade, however the impact of light limitation on chemical defenses has not been assessed. We quantified constitutive and jasmonate-induced phloem defenses and growth patterns of white fringetree and black ash under differential light conditions and related them to EAB larval performance. White fringetree had significantly lower constitutive and induced activities of peroxidase, polyphenol oxidase, β-glucosidase, chitinase and lignin content, but significantly higher gallic acid equivalent soluble phenolic, soluble sugar, and oleuropein concentrations compared to black ash. Multivariate analyses based on tissue chemical attributes displayed clear separation of species and induced defense responses. Further, EAB performed significantly worse on white fringetree than black ash, consistent with previous studies. Light limitation did not impact measured defenses or EAB larval performance, but it did decrease current year growth and increase photosynthetic efficiency. Overall our results suggest that phenolic profiles, metabolite abundance, and growth traits are important in mediating white fringetree resistance to EAB, and that short-term light limitation does not influence phloem chemistry or larval success.
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Data Availability
Data available at: https://github.com/mfriedman95/ChionanthusvirginicusEAB
References
Bartolini S, Leccese A, Andreini L (2014) Influence of canopy fruit location on morphological, histochemical and biochemical changes in two oil olive cultivars. Plant Biosyst - Int J Deal Asp Plant Biol 148:1221–1230. https://doi.org/10.1080/11263504.2014.980360
Barton KE, Koricheva J (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am Nat 175:481–493. https://doi.org/10.1086/650722
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Bryant JP, Chapin FS, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368. https://doi.org/10.2307/3544308
Calder WJ, Horn KJ, St. Clair SB (2011) Conifer expansion reduces the competitive ability and herbivore defense of aspen by modifying light environment and soil chemistry. Tree Physiol 31:582–591. https://doi.org/10.1093/treephys/tpr041
Cappaert D, McCullough DG, Poland TM, Siegert NW (2005) Emerald ash borer in North America: a research and regulatory challenge. Am Entomol 513 152-165 51:
Chen M-S (2008) Inducible direct plant defense against insect herbivores: a review. Insect Sci 15:101–114. https://doi.org/10.1111/j.1744-7917.2008.00190.x
Chen Y, Poland TM (2009) Interactive influence of leaf age, light intensity, and girdling on green ash foliar chemistry and emerald ash borer development. J Chem Ecol 35:806–815. https://doi.org/10.1007/s10886-009-9661-1
Cipollini D (2015) White fringetree as a novel larval host for emerald ash borer. J Econ Entomol 108:370–375. https://doi.org/10.1093/jee/tou026
Cipollini DF, Bergelson J (2000) Environmental and developmental regulation of trypsin inhibitor activity in Brassica napus. J Chem Ecol 26:1411–1422. https://doi.org/10.1023/A:1005540107957
Cipollini D, Peterson DL (2018) The potential for host switching via ecological fitting in the emerald ash borer-host plant system. Oecologia 187:507–519. https://doi.org/10.1007/s00442-018-4089-3
Cipollini D, Rigsby CM (2015) Incidence of infestation and larval success of emerald ash borer (Agrilus planipennis) on white fringetree (Chionanthus virginicus), Chinese fringetree (Chionanthus retusus), and devilwood (Osmanthus americanus). Environ Entomol 44:1375–1383. https://doi.org/10.1093/ee/nvv112
Cipollini D, Wang Q, Whitehill JGA, Powell JR, Bonello P, Herms DA (2011) Distinguishing defensive characteristics in the phloem of ash species resistant and susceptible to emerald ash borer. J Chem Ecol 37:450–459. https://doi.org/10.1007/s10886-011-9954-z
Erbilgin N (2019) Phytochemicals as mediators for host range expansion of a native invasive forest insect herbivore. New Phytol 221:1268–1278. https://doi.org/10.1111/nph.15467
Eyles A, Jones W, Riedl K, Cipollini D, Schwartz S, Chan K, Herms DA, Bonello P (2007) Comparative phloem chemistry of Manchurian (Fraxinus mandshurica) and two north American ash species (Fraxinus americana and Fraxinus pennsylvanica). J Chem Ecol 33:1430–1448. https://doi.org/10.1007/s10886-007-9312-3
Favaretto VF, Martinez CA, Soriani HH, Furriel RPM (2011) Differential responses of antioxidant enzymes in pioneer and late-successional tropical tree species grown under sun and shade conditions. Environ Exp Bot 70:20–28. https://doi.org/10.1016/j.envexpbot.2010.06.003
Felton GW, Summers CB, Mueller AJ (1994) Oxidative responses in soybean foliage to herbivory by bean leaf beetle and three-cornered alfalfa hopper. J Chem Ecol 20:639–650. https://doi.org/10.1007/BF02059604
Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci 14:10242–10297. https://doi.org/10.3390/ijms140510242
Haack RA, Benjamin DM, Haack KD (1983) Buprestidae, Cerambycidae, and Scolytidae associated with successive stages of Agrilus bilineatus (Coleoptera: Buprestidae) infestation of oaks in Wisconsin. 16:10
Haavik LJ, Coleman TW, Flint ML et al (2013) Agrilus auroguttatus (Coleoptera: Buprestidae) seasonal development within Quercus agrifolia (Fagales: Fagaceae) in southern California. Ann Entomol Soc am 1062 189-197 106:189–197. https://doi.org/10.1603/AN12112
Hamilton JG, Zangerl AR, DeLucia EH, Berenbaum MR (2001) The carbon–nutrient balance hypothesis: its rise and fall. Ecol Lett 4:86–95. https://doi.org/10.1046/j.1461-0248.2001.00192.x
Herms DA, McCullough DG (2014) Emerald ash borer invasion of North America: history, biology, ecology, impacts, and management. Annu Rev Entomol 59:13–30. https://doi.org/10.1146/annurev-ento-011613-162051
Iason GR, Hester AJ (1993) The response of heather (Calluna Vulgaris) to shade and nutrients--predictions of the carbon-nutrient balance hypothesis. J Ecol 81:75–80. https://doi.org/10.2307/2261225
Jensen SR, Franzyk H, Wallander E (2002) Chemotaxonomy of the Oleaceae: iridoids as taxonomic markers. Phytochemistry 60:213–231. https://doi.org/10.1016/S0031-9422(02)00102-4
Kitao M, Lei TT, Koike T, Tobita H, Maruyama Y (2006) Tradeoff between shade adaptation and mitigation of photoinhibition in leaves of Quercus mongolica and Acer mono acclimated to deep shade. Tree Physiol 26:441–448. https://doi.org/10.1093/treephys/26.4.441
Klooster WS, Gandhi KJK, Long LC, Perry K, Rice K, Herms D (2018) Ecological impacts of emerald ash borer in forests at the epicenter of the invasion in North America. Forests 9:250. https://doi.org/10.3390/f9050250
Komsta L (2011) Outliers: tests for outliers
Konno K, Hirayama C, Yasui H, Nakamura M (1999) Enzymatic activation of oleuropein: a protein crosslinker used as a chemical defense in the privet tree. Proc Natl Acad Sci 96:9159–9164. https://doi.org/10.1073/pnas.96.16.9159
Lawrence SD, Novak NG (2006) Expression of poplar chitinase in tomato leads to inhibition of development in Colorado potato beetle. Biotechnol Lett 28:593–599. https://doi.org/10.1007/s10529-006-0022-7
Lenth R (2019) Emmeans: estimated marginal means, aka least-squared means
Moreira-Vilar FC, Siqueira-Soares R de C, Finger-Teixeira A, et al (2014) The acetyl bromide method is faster, simpler and presents best recovery of lignin in different herbaceous tissues than Klason and thioglycolic acid methods. PLoS One 9:e110000. https://doi.org/10.1371/journal.pone.0110000
Muilenburg VL, Herms DA (2012) A review of bronze birch borer (Coleoptera: Buprestidae) life history, ecology, and management. Environ Entomol 41:1372–1385. https://doi.org/10.1603/EN12238
Muilenburg VL, Phelan PL, Bonello P, Herms DA (2011) Inter- and intra-specific variation in stem phloem phenolics of paper birch (Betula papyrifera) and European white birch (Betula pendula). J Chem Ecol 37:1193–1202. https://doi.org/10.1007/s10886-011-0028-z
Oksanen J, Blanchet FG, Friendly M, et al (2019) Vegan: community ecology package
Pedraza-Reyes M, Lopez-Romero E (1991) Chitinase activity in germinating cells of Mucor rouxii. Antonie Van Leeuwenhoek 59:183–189. https://doi.org/10.1007/BF00580658
Peterson DL, Cipollini D (2020) Larval performance of a major forest pest on novel hosts and the effect of stressors. Environ Entomol 49:482–488. https://doi.org/10.1093/ee/nvz160
Rigsby CM, Cipollini D, Amstutz EM, Smith TJ, Yoder JA (2013) Water conservation features of ova of Agrilus planipennis (Coleoptera: Buprestidae). Environ Entomol 42:363–369. https://doi.org/10.1603/EN12226
Rigsby CM, Herms DA, Bonello P, Cipollini D (2016) Higher activities of defense-associated enzymes may contribute to greater resistance of Manchurian ash to emerald ash borer than a closely related and susceptible congener. J Chem Ecol 42:782–792. https://doi.org/10.1007/s10886-016-0736-5
Rigsby CM, Villari C, Peterson DL, Herms DA, Bonello P, Cipollini D (2018) Girdling increases survival and growth of emerald ash borer larvae on Manchurian ash. Agric For Entomol 21:1–6. https://doi.org/10.1111/afe.12292
Romero-Segura C, Sanz C, Perez AG (2009) Purification and characterization of an olive fruit β-glucosidase involved in the biosynthesis of virgin olive oil phenolics. J Agric Food Chem 57:7983–7988. https://doi.org/10.1021/jf901293c
Rutledge CE, Arango-Velez A (2017) Larval survival and growth of emerald ash borer (Coleoptera: Buprestidae) on white ash and white fringetree saplings under well-watered and water-deficit conditions. Environ Entomol 46:243–250. https://doi.org/10.1093/ee/nvw080
Spadafora A, Mazzuca S, Chiappetta FF, Parise A, Perri E, Innocenti AM (2008) Oleuropein-specific-β-glucosidase activity marks the early response of olive fruits (Olea europaea) to mimed insect attack. Agric Sci China 7:703–712. https://doi.org/10.1016/S1671-2927(08)60105-4
Theis J, Schroda M (2016) Revisiting the photosystem II repair cycle. Plant Signal Behav 11:e1218587. https://doi.org/10.1080/15592324.2016.1218587
van Buuren S, Groothuis-Oudshoorn K (2011) Mice: multivariate imputation by chained equations in R. J Stat Softw 45:1–67
Velázquez-Palmero D, Romero-Segura C, García-Rodríguez R, Hernández ML, Vaistij FE, Graham IA, Pérez AG, Martínez-Rivas JM (2017) An oleuropein β-glucosidase from olive fruit is involved in determining the phenolic composition of virgin olive oil. Front Plant Sci 8:. https://doi.org/10.3389/fpls.2017.01902
Wallander E, Albert VA (2000) Phylogeny and classification of Oleaceae based on rps16 and trnL-F sequence data. Am J Bot 87:1827–1841. https://doi.org/10.2307/2656836
Wang X-Y, Yang Z-Q, Gould JR, Zhang YN, Liu GJ, Liu ES (2010) The biology and ecology of the emerald ash borer, Agrilus planipennis, in China. J Insect Sci 10:1–23. https://doi.org/10.1673/031.010.12801
War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320. https://doi.org/10.4161/psb.21663
Whitehill JGA, Opiyo SO, Koch JL, Herms DA, Cipollini DF, Bonello P (2012) Interspecific comparison of constitutive ash phloem phenolic chemistry reveals compounds unique to Manchurian ash, a species resistant to emerald ash borer. J Chem Ecol 38:499–511. https://doi.org/10.1007/s10886-012-0125-7
Whitehill JGA, Rigsby C, Cipollini D, Herms DA, Bonello P (2014) Decreased emergence of emerald ash borer from ash treated with methyl jasmonate is associated with induction of general defense traits and the toxic phenolic compound verbascoside. Oecologia 176:1047–1059. https://doi.org/10.1007/s00442-014-3082-8
Yang Y, Han C, Liu Q, Lin B, Wang J (2008) Effect of drought and low light on growth and enzymatic antioxidant system of Picea asperata seedlings. Acta Physiol Plant 30:433–440. https://doi.org/10.1007/s11738-008-0140-z
Acknowledgments
We thank Donnie Peterson, Emily Ellison, Alicia Goffe, and Juan Manuel Perilla Lopez for assistance in both field and laboratory components of this experiment. This project was funded in part by USDA-APHIS Cooperative Agreement 15-8130-0539-CA and the Graduate Student Association of Wright State University.
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Funding for this project was provided in part by USDA-APHIS Cooperative Agreement 15–8130-0539-CA.
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Michael S. Friedman and Don Cipollini contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Michael S. Friedman, Chad M. Rigsby, and Don Cipollini. The first draft of the manuscript was written by Michael S. Friedman. All authors read and approved the final manuscript.
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Friedman, M.S., Rigsby, C.M. & Cipollini, D. Light Limitation Impacts Growth but Not Constitutive or Jasmonate Induced Defenses Relevant to Emerald Ash Borer (Agrilus planipennis) in White Fringetree (Chionanthus virginicus) or Black Ash (Fraxinus nigra). J Chem Ecol 46, 1117–1130 (2020). https://doi.org/10.1007/s10886-020-01223-0
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DOI: https://doi.org/10.1007/s10886-020-01223-0