Abstract
Sorghum (Sorghum bicolor (L.) Moench) brown midrib (bmr) mutant lines have reduced levels of lignin, which is a potentially useful trait for bioenergy production, but the effects of this trait on insect and plant pathogen interactions are unknown under field conditions. Field-grown bmr6, bmr12, and wild-type (WT) plants were examined for insect and disease damage. In most cases, observed frequency, population, or leaf area damage caused by insects or pathogens on bmr6 or bmr12 plants were not greater than those observed on WT plants in the field or laboratory assays. European corn borers [Ostrinia nubilalis (Hübner)(Lepidoptera: Pyralidae)] often caused lower amounts of leaf damage to bmr6 leaves compared to bmr12 and sometimes WT leaves in the field study. Leaf damage by corn earworms [Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)] and fall armyworms [Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae)] in laboratory assays was often lower for bmr versus WT leaves. Incidence of disease lesions was significantly higher on bmr6 compared to WT plants for one of three samplings in 2011, but the opposite trend was observed overall in 2012 and no significant differences were noted in 2013. When corn earworms and fall armyworms were fed the excised pith, bmr6 and/or bmr12 pith caused significant morality to one or both insect species in all 3 years. Damage variability between the 3 years may have been due to hotter and drier than normal conditions in 2012. Thus, bmr lines of sorghum suitable for bioenergy production have potential for sustainable production in the field.

Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to field. J Exp Bot 63:3523–3543
Bhuiyan NH, Selvaraj G, Wei Y, King J (2009a) Role of lignification in plant defense. Plant Signal Behav 4:158–159
Bhuiyan NH, Selvaraj G, Wei Y, King J (2009b) Gene expression profiling and silencing reveal that monolignol biosynthesis plays a critical role in penetration defense in wheat against powdery mildew invasions. J Exp Bot 60:509–521
Bout S, Vermerris W (2003) A candidate-gene approach to clone the sorghum brown midrib gene encoding caffeic acid O-methyl transferase. Mol Genet Genomic 269:205–214
Brodeur-Campbell SE, Vucetich JA, Richter DL, Waite TA, Rosemier JN, Tsai C-J (2006) Insect herbivory on low-lignin transgenic aspen. Environ Entomol 35:1696–1701
Cheng W-N, Lei J-X, Rooney WL, Liu T-L, Zhu-Salzman K (2013) High basal defense gene expression determines sorghum resistance to the whorl-feeding insect southwestern corn borer. Insect Sci 20:307–317
Dien BS, Sarath G, Pedersen JF, Sattler SE, Chen H, Funnell-Harris DL, Nichols NN, Cotta MA (2009) Improved sugar conversion and ethanol yield for forage sorghum (Sorghum bicolor L. Moench) lines with reduced lignin contents. Bioenerg Res 2:153–164
Djanaguiraman M, Prasad PVV, Al-Khatib K (2011) Ethylene perception inhibitor 1-MCP decreases oxidative damage of leaves through enhanced antioxidant defense mechanisms in soybean plants grown under high temperature stress. Environ Exp Bot 71:215–223
Dowd PF (1988) Toxicological and biochemical interactions of the fungal metabolites fusaric acid and kojic acid with xenobiotics in Heliothis zea (F.) and Spodoptera frugiperda (J. E. Smith). Pestic Biochem Physiol 32:123–134
Dowd PF, Sattler SE (2015) Corn earworm (Helicoverpa zea) and fall armyworm (Spodoptera frugiperda) responses to sorghum (Sorghum bicolor) tissues from lowered lignin lines. J Insect Sci. doi:10.1093/jisesa/ieu162
Dowd PF, White DG (2002) Corn earworm, Helicoverpa zea (Lepidoptera: Noctuidae) and other insect associated resistance in the maize inbred Tex6. J Econ Entomol 95:628–634
Dowd PF, Johnson ET, Pinkerton TS (2007) Oral toxicity of β-N-acetyl hexosaminidase to insects. J Agric Food Chem 55:3421–3428
Dowd PF, Sarath G, Mitchell RB, Saathoff AJ, Vogel KP (2013) Insect resistance of a full sib family of tetraploid switchgrass Panicum virgatum L. with varying lignin levels. Genet Resour Crop Evol 60:975–984
Duncan RR (1996) Breeding and improvement of forage sorghum for the tropics. Adv Agron 57:161–185
Frederiksen RA, Odvody GN (2000) Compendium of sorghum diseases. APS Press, St. Paul
Funnell-Harris DL, Pedersen JF, Sattler SE (2010) Alteration in the lignin biosynthesis restricts growth of Fusarium spp. in brown midrib sorghum. Phytopathology 100:671–681
Funnell-Harris DL, Sattler SE, Pedersen JF (2014) Response of Fusarium thapsinum to sorghum brown midrib lines and to phenolic metabolites. Plant Dis 98:1300–1308
Grinnan R, Carter TE Jr, Johnson MTJ (2013) Effects of drought, temperature, herbivory and genotype on plant-insect interactions in soybean (Glycine max). Arthropod Plant Interact. doi:10.1007/s1:1829-012-9234-x
Huang Y, Sharma HC, Dhillon MK (2013) Bridging conventional and molecular genetics of sorghum insect resistance. In: Patterson AE (ed) Genomics of the Saccharinae. Springer, New York, pp 367–389
Koornneef A, Pieterse CMJ (2008) Cross-talk in defense signaling. Plant Physiol 146:839–844
Krothapalli KE, Buescher M, Li X, Brown E, Chappel C, Dilkes PB, Tuinstra MR (2013) Forward genetics by genome sequencing reveals that rapid cyanide release deters insect herbivory of Sorghum bicolor. Genetics 195:309–318
Kuokkanen K, Julkunen-Tiitto R, Keinänen M, Niemelä P, Tahvanainen J (2001) The effect of elevated CO2 and temperature on the secondary chemistry of Betula pendula seedlings. Trees 15:378–384
Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16:319–331
Lo SC, Weiergang I, Bonham C, Hipskind L, Wood K, Nicholson RL (1996) Phytoalexin accumulation in sorghum: identification of a methyl ether of luteolinidin. Physiol Mol Plant Pathol 49:21–31
Lordello ALL, Lara FM, Parra JRP (1980) Food preference among sorghums in Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) under laboratory conditions. An Soc Entomol Bras 9:219–241
Maimbo M, Ohnishi K, Hikichi Y, Yoshioka H, Kiba A (2007) Induction of a small heat shock protein and its functional roles in Nicotiana plants in the defense response against Ralstonia solanacearum. Plant Physiol 145:1588–1599
Metcalf RL, Metcalf RM (1993) Destructive and useful insects. McGraw Hill, New York
Moore JW, Ditmore M, TeBeest DL (2010) Development of anthracnose on grain sorghum hybrids inoculated with recently described pathotypes of Colletotrichum sublineolum found in Arkansas. Plant Dis 94:589–595
Mosolov VV, Valueva TA (2011) Inhibitors of proteolytic enzymes under abiotic stresses in plants. Appl Biochem Microbiol 47:501–507
Palmer NA, Sattler SE, Saathoff AJ, Funnell D, Pedersen JF, Sarath G (2008) Genetic background impacts soluble and cell wall-bound aromatics in brown midrib mutants of sorghum. Planta 229:113–127
Pedersen JF, Vogel KP, Funnell DL (2005) Impact of reduced lignin on plant fitness. Crop Sci 45:812–819
Pedersen JF, Funnell DL, Toy JJ, Oliver AL, Grant RJ (2006) Registration of twelve grain sorghum genetic stocks near-isogenic for the brown midrib genes bmr-6 and bmr-12. Crop Sci 46:491–492
Peltier AJ, Hatfield RD, Grau CR (2009) Soybean stem lignin concentration relates to resistance to Sclerotinia sclerotiorum. Plant Dis 93:149–154
Roy BA, Gusewell S, Harte J (2004) Response of plant pathogens and herbivores to a warming experiment. Ecology 85:2570–2581
Saballos A, Ejeta G, Sanchez E, Kang C, Vermerris W (2009) A genomewide analysis of the cinnamyl alcohol dehydrogenase family in sorghum (Sorghum bicolor (L.) Moench) identified SBCAD2 as the brown midrib 6 gene. Genetics 181:783–785
Santiago R, Barros-Rios J, Malvar RA (2013) Impact of cell wall composition on maize resistance to pests and diseases. Int J Mol Sci 14:6960–6980
Sattler SE, Saathoff AJ, Haas EJ, Palmer NA, Funnell-Harris DL, Sarath G, Pedersen JF (2009) A nonsense mutation in a cinnamyl alcohol dehydrogenase gene is responsible for the sorghum brown midrib 6 phenotype. Plant Physiol 150:584–585
Sun J-Q, Jiang H-L, Li C-Y (2011) Systemin/jasmonate-mediated systemic defense signaling in tomato. Mol Plant 4:607–615
Swain T (1979) Tannins and lignins. In: Rosenthal GA, Janzen DH (eds) Herbivores, their interaction with plant secondary metabolites. Academic, New York
Tesso T, Perumal R, Little CR, Adeyanju A, Radwan GL, Prom LK, Magill CW (2012) Sorghum pathology and biotechnology: a fungal disease perspective: part II. Anthracnose, stalk rot and downy mildew. Eur J Plant Sci Biotechnol 6:31–44
United States Department of Energy (2011) U.S. billion ton update: biomass supply for a bioenergy and bioproducts industry. In: Perlak R. D, Stokes B. J (eds.). ORNL/TM-2011/2014. Oak Ridge National Laboratory, Oak Ridge
Van den Berg J, Van Rensburg GDH, Van der Westhuilzen MC (1994) Host-plant resistance and chemical control of Chilo partellus (Swinhoe) and Busseola fusca (Fuller) in an integrated pest management system on grain sorghum. Crop Prot 13:308–310
Vance CP, Kirk TK, Sherwood RT (1980) Lignification as a mechanism of disease resistance. Annu Rev Phytopathol 18:259–288
Wheeler GS, Slansky F (1991) Compensatory response of the fall armyworm (Spodoptera frugiperda) when fed water and cellulose-diluted diets. Physiol Entomol 16:361–374
Zhao Q, Dixon RA (2014) Altering the cell wall and its impact on plant disease: from forage to bioenergy. Annu Rev Phytopathol 52:69–91
Acknowledgments
We thank A. Cranford, Z. Demkovitch, and D. Lee for technical assistance, and A. P Rooney for comments on prior versions of the manuscript. This work was supported by Agricultural Food Research Institute Grant (No. 2011-67009-30026) from the National Institute of Food and Agriculture, and funding of the base Agricultural Research Service projects.
Funding
This study was funded by Agricultural Food Research Institute award number 2011-67009-30026 from the National Institute of Food and Agriculture, and funding from the base Agricultural Research Service projects.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Disclaimer
Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. This article is in the public domain and not copyrightable. It may be freely reprinted with customary crediting of source. The U.S. Department of Agriculture (USDA) prohibits discrimination in all its programs and activities on the basis of race, color, national origin, age, disability, and where applicable, sex, marital status, familial status, parental status, religion, sexual orientation, genetic information, political beliefs, reprisal, or because all or part of an individual’s income is derived from any public assistance program. (Not all prohibited bases apply to all programs.) Persons with disabilities who require alternative means for communication of program information (Braille, large print, audiotape, etc.) should contact USDA’s TARGET Center at (202) 720-2600 (voice and TDD). To file a complaint of discrimination, write to USDA, Director, Office of Civil Rights, 1400 Independence Avenue, S.W., Washington, DC. 20250-9410, or call (800) 795-3272 (voice) or (202) 720-6382 (TDD). USDA is an equal opportunity provider and employer.
Additional information
Communicated by J. Gross.
Rights and permissions
About this article
Cite this article
Dowd, P.F., Funnell-Harris, D.L. & Sattler, S.E. Field damage of sorghum (Sorghum bicolor) with reduced lignin levels by naturally occurring insect pests and pathogens. J Pest Sci 89, 885–895 (2016). https://doi.org/10.1007/s10340-015-0728-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-015-0728-1


