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Plant function and evolutionary biology
RESEARCH ARTICLE

Identification of an orthologous clade of peroxidases that respond to feeding by greenbugs (Schizaphis graminum) in C4 grasses

Erin D. Scully A , Teresa Donze-Reiner B , Haichuan Wang C , Thomas E. Eickhoff C D , Frederick Baxendale C , Paul Twigg E , Frank Kovacs F , Tiffany Heng-Moss C , Scott E. Sattler G and Gautam Sarath G H
+ Author Affiliations
- Author Affiliations

A Stored Product Insect and Engineering Research Unit, Center for Grain and Animal Health Research USDA-ARS, Manhattan, KS 66502, USA.

B Department of Biology, West Chester University, West Chester, PA 19382, USA.

C Department of Entomology, University of Nebraska-Lincoln, Lincoln, NE 68583, USA.

D Monsanto Company, 800 North Lindbergh Blvd, St Louis, MO 63167, USA.

E Department of Biology, University of Nebraska-Kearney, Kearney, NE 68849, USA.

F Department of Chemistry, University of Nebraska-Kearney, Kearney, NE 68849, USA.

G Grain, Forage and Bioenergy Research Unit, USDA-ARS, Lincoln, NE 68583, USA.

H Corresponding Author. Email: gautam.sarath@ars.usda.gov

Functional Plant Biology 43(12) 1134-1148 https://doi.org/10.1071/FP16104
Submitted: 17 March 2016  Accepted: 29 July 2016   Published: 26 August 2016

Abstract

Knowledge of specific peroxidases that respond to aphid herbivory is limited in C4 grasses, but could provide targets for improving defence against these pests. A sorghum (Sorghum bicolor (L.) Moench) peroxidase (SbPrx-1; Sobic.002G416700) has been previously linked to biotic stress responses, and was the starting point for this study. Genomic analyses indicated that SbPrx-1 was part of a clade of five closely related peroxidase genes occurring within a ~30 kb region on chromosome 2 of the sorghum genome. Comparison of this ~30-kb region to syntenic regions in switchgrass (Panicum virgatum L.) and foxtail millet (Setaria italica L.) identified similar related clusters of peroxidases. Infestation of a susceptible sorghum cultivar with greenbugs (Shizaphis graminum Rondani) induced three of the five peroxidases. Greenbug infestation of switchgrass and foxtail millet plants showed similar inductions of peroxidases. SbPrx-1 was also induced in response to aphid herbivory in a greenbug-resistant sorghum line, Cargill 607E. These data indicate that this genomic region of C4 grasses could be valuable as a marker to assess potential insect resistance in C4 grasses.

Additional keywords: defense, defence, foxtail millet, greenbugs, plant resistance, sorghum, switchgrass, synteny.


References

Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105.
ProtTest: selection of best-fit models of protein evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsl2ns7Y%3D&md5=4fbffa8df2714f9a063729160ff0d73eCAS | 15647292PubMed |

Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 55, 539–552.
Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative.Crossref | GoogleScholarGoogle Scholar | 16785212PubMed |

Bailey TL (2011) DREME: motif discovery in transcription factor ChIP-seq data. Bioinformatics 27, 1653–1659.
DREME: motif discovery in transcription factor ChIP-seq data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntFGkurg%3D&md5=6be22d66ce41bc82b6aecaafd46601ebCAS | 21543442PubMed |

Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Research 34, W369–W373.
MEME: discovering and analyzing DNA and protein sequence motifs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1yiurc%3D&md5=c847381010fea50204e04d6dbffde1aaCAS | 16845028PubMed |

Barbehenn R, Dukatz C, Holt C, Reese A, Martiskainen O, Salminen JP, Yip L, Tran L, Constabel CP (2010) Feeding on poplar leaves by caterpillars potentiates foliar peroxidase action in their guts and increases plant resistance. Oecologia 164, 993–1004.
Feeding on poplar leaves by caterpillars potentiates foliar peroxidase action in their guts and increases plant resistance.Crossref | GoogleScholarGoogle Scholar | 20680646PubMed |

Bennetzen JL, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli AC, Estep M, Feng L, Vaughn JN, Grimwood J, Jenkins J, Barry K, Lindquist E, Hellsten U, Deshpande S, Wang X, Wu X, Mitros T, Triplett J, Yang X, Ye CY, Mauro-Herrera M, Wang L, Li P, Sharma M, Sharma R, Ronald PC, Panaud O, Kellogg EA, Brutnell TP, Doust AN, Tuskan GA, Rokhsar D, Devos KM (2012) Reference genome sequence of the model plant Setaria. Nature Biotechnology 30, 555–561.
Reference genome sequence of the model plant Setaria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmvFCitL0%3D&md5=c84f144615b3314b86edb5287379e30aCAS | 22580951PubMed |

Berman H, Henrick K, Nakamura H (2003) Announcing the worldwide Protein Data Bank. Nature Structural Biology 10, 980
Announcing the worldwide Protein Data Bank.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptFOmsbY%3D&md5=74ab3e1732e45077f0a6f5065554cbc8CAS | 14634627PubMed |

Carmona D, Fornoni J (2013) Herbivores can select for mixed defensive strategies in plants. New Phytologist 197, 576–585.
Herbivores can select for mixed defensive strategies in plants.Crossref | GoogleScholarGoogle Scholar | 23171270PubMed |

Chaman ME, Corcuera LJ, Zuniga GE, Cardemil L, Argandona VH (2001) Induction of soluble and cell wall peroxidases by aphid infestation in barley. Journal of Agricultural and Food Chemistry 49, 2249–2253.
Induction of soluble and cell wall peroxidases by aphid infestation in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisl2ktbY%3D&md5=bd71634fb01fc0e54c869466e5cb69d6CAS | 11368584PubMed |

Distelfeld A, Pearce SP, Avni R, Scherer B, Uauy C, Piston F, Slade A, Zhao R, Dubcovsky J (2012) Divergent functions of orthologous NAC transcription factors in wheat and rice. Plant Molecular Biology 78, 515–524.
Divergent functions of orthologous NAC transcription factors in wheat and rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1Sls7k%3D&md5=78cda751fee551e9d59f52cbd06a8e20CAS | 22278768PubMed |

Dixon P (2003) VEGAN, a package of R functions for community ecology. Journal of Vegetation Science 14, 927–930.
VEGAN, a package of R functions for community ecology.Crossref | GoogleScholarGoogle Scholar |

Dogramaci M, Mayo ZB, Wright R, Reese J (2007) Categories of resistance, antibiosis and tolerance, to biotype I greenbug (Schizaphis graminum (Rondani) Homoptera: Aphididae) in four sorghum (Sorghum bicolor (L.) Moench. Poales: Gramineae) hybrids. Journal of the Kansas Entomological Society 80, 183–191.
Categories of resistance, antibiosis and tolerance, to biotype I greenbug (Schizaphis graminum (Rondani) Homoptera: Aphididae) in four sorghum (Sorghum bicolor (L.) Moench. Poales: Gramineae) hybrids.Crossref | GoogleScholarGoogle Scholar |

Dowd PF, Lagrimini LM (2006) Examination of the biological effects of high anionic peroxidase production in tobacco plants grown under field conditions. I. Insect pest damage. Transgenic Research 15, 197–204.
Examination of the biological effects of high anionic peroxidase production in tobacco plants grown under field conditions. I. Insect pest damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt1ykur8%3D&md5=3363846101628dcb84c7a2c11b4602c7CAS | 16604460PubMed |

Dowd PF, Holmes RA, Pinkerton TS, Johnson ET, Lagrimini LM, Boston RS (2006) Relative activity of a tobacco hybrid expressing high levels of a tobacco anionic peroxidase and maize ribosome-inactivating protein against Helicoverpa zea and Lasioderma serricorne. Journal of Agricultural and Food Chemistry 54, 2629–2634.
Relative activity of a tobacco hybrid expressing high levels of a tobacco anionic peroxidase and maize ribosome-inactivating protein against Helicoverpa zea and Lasioderma serricorne.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xit1Oku7w%3D&md5=02bfdb3c94d9f8ebac421d5c7b925da0CAS | 16569054PubMed |

Franzen LD, Gutsche AR, Heng-Moss TM, Higley LG, Sarath G, Burd JD (2007) Physiological and biochemical responses of resistant and susceptible wheat to injury by Russian wheat aphid. Journal of Economic Entomology 100, 1692–1703.
Physiological and biochemical responses of resistant and susceptible wheat to injury by Russian wheat aphid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Clt7jO&md5=d8bd06325379124f2be2f775100303acCAS | 17972650PubMed |

Furch ACU, van Bel AJE, Will T (2015) Aphid salivary proteases are capable of degrading sieve-tube proteins. Journal of Experimental Botany 66, 533–539.
Aphid salivary proteases are capable of degrading sieve-tube proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVGjsrrL&md5=677de6181d3520399a3a43d83f994613CAS |

Goodstein DM, Shu SQ, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research 40, D1178–D1186.
Phytozome: a comparative platform for green plant genomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs12htbjE&md5=ecfe37e12f00b4aaf4f361e191ef246eCAS | 22110026PubMed |

Gulsen O, Eickhoff T, Heng-Moss T, Shearman R, Baxendale F, Sarath G, Lee D (2010) Characterization of peroxidase changes in resistant and susceptible warm-season turfgrasses challenged by Blissus occiduus. Arthropod-Plant Interactions 4, 45–55.
Characterization of peroxidase changes in resistant and susceptible warm-season turfgrasses challenged by Blissus occiduus.Crossref | GoogleScholarGoogle Scholar |

Gupta SK, Rai AK, Kanwar SS, Chand D, Singh NK, Sharma TR (2012) The single functional blast resistance gene Pi54 activates a complex defence mechanism in rice. Journal of Experimental Botany 63, 757–772.
The single functional blast resistance gene Pi54 activates a complex defence mechanism in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1CnsA%3D%3D&md5=441a6a5ad2010990ddd99e5448af5679CAS | 22058403PubMed |

Gutsche A, Heng-Moss T, Sarath G, Twigg P, Xia Y, Lu G, Mornhinweg D (2009a) Gene expression profiling of tolerant barley in response to Diuraphis noxia (Hemiptera: Aphididae) feeding. Bulletin of Entomological Research 99, 163–173.
Gene expression profiling of tolerant barley in response to Diuraphis noxia (Hemiptera: Aphididae) feeding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVKgsr4%3D&md5=7ac4528863d2e41c65f1c803fff78a66CAS | 18840314PubMed |

Gutsche AR, Heng-Moss TM, Higley LG, Sarath G, Mornhinweg DW (2009b) Physiological responses of resistant and susceptible barley, Hordeum vulgare to the Russian wheat aphid, Diurpahis noxia (Mordvilko). Arthropod-Plant Interactions 3, 233–240.
Physiological responses of resistant and susceptible barley, Hordeum vulgare to the Russian wheat aphid, Diurpahis noxia (Mordvilko).Crossref | GoogleScholarGoogle Scholar |

Heng-Moss T, Sarath G, Baxendale F, Novak D, Bose S, Ni X, Quisenberry S (2004) Characterization of oxidative enzyme changes in buffalograsses challenged by Blissus occiduus. Journal of Economic Entomology 97, 1086–1095.
Characterization of oxidative enzyme changes in buffalograsses challenged by Blissus occiduus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvVCjsL8%3D&md5=aa73fb50ebb9ae32f85aa6953ba4ad5aCAS | 15279295PubMed |

Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Research 27, 297–300.
Plant cis-acting regulatory DNA elements (PLACE) database: 1999.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXpsVKgug%3D%3D&md5=4f82a147abb173f8792b91f9969bc5f5CAS | 9847208PubMed |

Ibraheem F, Gaffoor I, Tan QX, Shyu CR, Chopra S (2015) A sorghum MYB transcription factor induces 3-deoxyanthocyanidins and enhances resistance against leaf blights in maize. Molecules 20, 2388–2404.
A sorghum MYB transcription factor induces 3-deoxyanthocyanidins and enhances resistance against leaf blights in maize.Crossref | GoogleScholarGoogle Scholar | 25647576PubMed |

Kayser JP, Kim JG, Cerny RL, Vallet JL (2006) Global characterization of porcine intrauterine proteins during early pregnancy. Reproduction 131, 379–388.
Global characterization of porcine intrauterine proteins during early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFalsbo%3D&md5=9fb593146c5a2c3143f6368d44d5e115CAS | 16452731PubMed |

Kerchev PI, Fenton B, Foyer CH, Hancock RD (2012) Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant, Cell & Environment 35, 441–453.
Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtVKnt74%3D&md5=d3a1e9925948d5765022659ed18f8813CAS |

Koch KG, Fithian R, Heng-Moss TM, Bradshaw JD, Sarath G, Spilker C (2014) Evaluation of tetraploid switchgrass (Poales: Poaceae) populations for host suitability and differential resistance to four cereal aphids. Journal of Economic Entomology 107, 424–431.
Evaluation of tetraploid switchgrass (Poales: Poaceae) populations for host suitability and differential resistance to four cereal aphids.Crossref | GoogleScholarGoogle Scholar | 24665729PubMed |

Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics 9, 299–306.
MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpt1artrg%3D&md5=102f499c7f5eb362d1ee7cd59ebf7717CAS | 18417537PubMed |

Lazebnik J, Frago E, Dicke M, van Loon JJA (2014) Phytohormone mediation of interactions between herbivores and plant pathogens. Journal of Chemical Ecology 40, 730–741.
Phytohormone mediation of interactions between herbivores and plant pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1WksbrN&md5=923cb2f064a4e2bdbc92bd2e3df88390CAS | 25059974PubMed |

Lei JX, Finlayson SA, Salzman RA, Shan LB, Zhu-Salzman K (2014) BOTRYTIS-INDUCED KINASE1 modulates Arabidopsis resistance to green peach aphids via PHYTOALEXIN DEFICIENT4. Plant Physiology 165, 1657–1670.
BOTRYTIS-INDUCED KINASE1 modulates Arabidopsis resistance to green peach aphids via PHYTOALEXIN DEFICIENT4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlKntbnI&md5=1f152628076fab2cc521c8a25aa21b72CAS |

Louis J, Shah J (2013) Arabidopsis thaliana-Myzus persicae interaction: shaping the understanding of plant defense against phloem-feeding aphids. Frontiers in Plant Science 4, 213
Arabidopsis thaliana-Myzus persicae interaction: shaping the understanding of plant defense against phloem-feeding aphids.Crossref | GoogleScholarGoogle Scholar | 23847627PubMed |

Mai VC, Bednarski W, Borowiak-Sobkowiak B, Wilkaniec B, Samardakiewicz S, Morkunas I (2013) Oxidative stress in pea seedling leaves in response to Acyrthosiphon pisum infestation. Phytochemistry 93, 49–62.
Oxidative stress in pea seedling leaves in response to Acyrthosiphon pisum infestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlsVKjt7w%3D&md5=a4986d55e50d0099f51777f0ab479138CAS | 23566717PubMed |

Marchi-Werle L, Heng-Moss TM, Hunt TE, Baldin ELL, Baird LM (2014) Characterization of peroxidase changes in tolerant and susceptible soybeans challenged by soybean aphid (Hemiptera: Aphididae). Journal of Economic Entomology 107, 1985–1991.
Characterization of peroxidase changes in tolerant and susceptible soybeans challenged by soybean aphid (Hemiptera: Aphididae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFOjtLbK&md5=28809033fdc6c6cd0b723015e0618d19CAS | 26309290PubMed |

Massa AN, Wanjugi H, Deal KR, O’Brien K, You FM, Maiti R, Chan AP, Gu YQ, Luo MC, Anderson OD, Rabinowicz PD, Dvorak J, Devos KM (2011) Gene space dynamics during the evolution of Aegilops tauschii, Brachypodium distachyon, Oryza sativa, and Sorghum bicolor genomes. Molecular Biology and Evolution 28, 2537–2547.
Gene space dynamics during the evolution of Aegilops tauschii, Brachypodium distachyon, Oryza sativa, and Sorghum bicolor genomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFShu7fL&md5=a24984fcb1b5b3ccdb85fc51b35db029CAS | 21470968PubMed |

Michels GJ, Burd JD (2007) IPM case studies: sorghum. In ‘Aphids as crop pests’. (Eds HF Emden, R van Harrington) pp. 627–637. (CABI International: Walllingford, UK)

Mika A, Boenisch MJ, Hopff D, Luthje S (2010) Membrane-bound guaiacol peroxidases from maize (Zea mays L.) roots are regulated by methyl jasmonate, salicylic acid, and pathogen elicitors. Journal of Experimental Botany 61, 831–841.
Membrane-bound guaiacol peroxidases from maize (Zea mays L.) roots are regulated by methyl jasmonate, salicylic acid, and pathogen elicitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVSrurk%3D&md5=419c83932b957eb7ccc9d6230b562defCAS | 20032108PubMed |

Moloi MJ, van der Westhuizen AJ (2008) Antioxidative enzymes and the Russian wheat aphid (Diuraphis noxia) resistance response in wheat (Triticum aestivum). Plant Biology 10, 403–407.
Antioxidative enzymes and the Russian wheat aphid (Diuraphis noxia) resistance response in wheat (Triticum aestivum).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslaisrw%3D&md5=031485e355764ac394a00eadff0c4aa9CAS | 18426488PubMed |

Ni X, Quisenberry SS, Heng-Moss T, Markwell J, Sarath G, Klucas R, Baxendale F (2001) Oxidative responses of resistant and susceptible cereal leaves to symptomatic and nonsymptomatic cereal aphid (Hemiptera: Aphididae) feeding. Journal of Economic Entomology 94, 743–751.
Oxidative responses of resistant and susceptible cereal leaves to symptomatic and nonsymptomatic cereal aphid (Hemiptera: Aphididae) feeding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkvFegu7w%3D&md5=ac5dcfffa8b6808db1477b6fc0f9cdb7CAS | 11425032PubMed |

Ostlund G, Schmitt T, Forslund K, Kostler T, Messina DN, Roopra S, Frings O, Sonnhammer ELL (2010) InParanoid 7: new algorithms and tools for eukaryotic orthology analysis. Nucleic Acids Research 38, D196–D203.
InParanoid 7: new algorithms and tools for eukaryotic orthology analysis.Crossref | GoogleScholarGoogle Scholar | 19892828PubMed |

Padmaja PG, Shwetha BL, Swetha G, Patil JV (2014) Oxidative enzyme changes in sorghum infested by shoot fly. Journal of Insect Science 14, 193
Oxidative enzyme changes in sorghum infested by shoot fly.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2Mzmt1Gjsg%3D%3D&md5=522bd6a68e56dc580809fdab36e7954eCAS | 25480976PubMed |

Palmer NA, Saathoff AJ, Waters BM, Donze T, Heng-Moss TM, Twigg P, Tobias CM, Sarath G (2014) Global changes in mineral transporters in tetraploid switchgrasses (Panicum virgatum L.). Frontiers in Plant Science 4, 549
Global changes in mineral transporters in tetraploid switchgrasses (Panicum virgatum L.).Crossref | GoogleScholarGoogle Scholar | 24427165PubMed |

Passardi F, Longet D, Penel C, Dunand C (2004a) The class III peroxidase multigenic family in rice and its evolution in land plants. Phytochemistry 65, 1879–1893.
The class III peroxidase multigenic family in rice and its evolution in land plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVCjtrc%3D&md5=d2a84eb9753a070ae53fac5043f3eaf4CAS | 15279994PubMed |

Passardi F, Penel C, Dunand C (2004b) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends in Plant Science 9, 534–540.
Performing the paradoxical: how plant peroxidases modify the cell wall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovFWrtL4%3D&md5=c51a5125a68d2499a14bd1b807682994CAS | 15501178PubMed |

Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Reports 24, 255–265.
Peroxidases have more functions than a Swiss army knife.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmt1Wgtbo%3D&md5=dea351c4dc16f4479f8a0e1767408de9CAS | 15856234PubMed |

Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF chimera – a visualization system for exploratory research and analysis. Journal of Computational Chemistry 25, 1605–1612.
UCSF chimera – a visualization system for exploratory research and analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvVOhsbs%3D&md5=c91c53655050437850d825e19f9fdbc7CAS | 15264254PubMed |

Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with 4 different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384–394.
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with 4 different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkvFehtL4%3D&md5=80c9357b607f9ffe3581da2661975d73CAS |

Pratt LH, Liang C, Shah M, Sun F, Wang H, Reid SP, Gingle AR, Paterson AH, Wing R, Dean R, Klein R, Nguyen HT, Ma HM, Zhao X, Morishige DT, Mullet JE, Cordonnier-Pratt MM (2005) Sorghum expressed sequence tags identify signature genes for drought, pathogenesis, and skotomorphogenesis from a milestone set of 16,801 unique transcripts. Plant Physiology 139, 869–884.
Sorghum expressed sequence tags identify signature genes for drought, pathogenesis, and skotomorphogenesis from a milestone set of 16,801 unique transcripts.Crossref | GoogleScholarGoogle Scholar | 16169961PubMed |

Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nature Protocols 5, 725–738.
I-TASSER: a unified platform for automated protein structure and function prediction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksVahs74%3D&md5=902147331ca40523202e726ff2ed5a22CAS | 20360767PubMed |

Saathoff AJ, Donze T, Palmer NA, Bradshaw J, Heng-Moss T, Twigg P, Tobias CM, Lagrimini M, Sarath G (2013) Towards uncovering the roles of switchgrass peroxidases in plant processes. Frontiers in Plant Science 4, 202
Towards uncovering the roles of switchgrass peroxidases in plant processes.Crossref | GoogleScholarGoogle Scholar | 23802005PubMed |

Sanyal A, Lajoie BR, Jain G, Dekker J (2012) The long-range interaction landscape of gene promoters. Nature 489, 109–113.
The long-range interaction landscape of gene promoters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlGnsLnM&md5=80cdeec4d2d708b4d42eb3d2418d5e0dCAS | 22955621PubMed |

Schnable JC (2015) Genome evolution in maize: from genomes back to genes. Annual Review of Plant Biology 66, 329–343.
Genome evolution in maize: from genomes back to genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVajtbjP&md5=3b309beffbf1a7faa16a7da2314957a1CAS | 25494463PubMed |

Schnable JC, Freeling M, Lyons E (2012) Genome-wide analysis of syntenic gene deletion in the grasses. Genome Biology and Evolution 4, 265–277.
Genome-wide analysis of syntenic gene deletion in the grasses.Crossref | GoogleScholarGoogle Scholar | 22275519PubMed |

Scully ED, Gries T, Sarath G, Palmer NA, Baird L, Serapiglia MJ, Dien BS, Boateng AA, Ge Z, Funnell-Harris DL, Twigg P, Clemente TE, Sattler SE (2016) Overexpression of SbMyb60 impacts phenylpropanoid biosynthesis and alters secondary cell wall composition in Sorghum bicolor. The Plant Journal 85, 378–395.
Overexpression of SbMyb60 impacts phenylpropanoid biosynthesis and alters secondary cell wall composition in Sorghum bicolor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhs1Ojt70%3D&md5=e2e18fbc8c7a1d1ce6ede75222e77787CAS | 26712107PubMed |

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. Journal of Chemical Ecology 38, 1247–1263.
Effects of elevated peroxidase levels and corn earworm feeding on gene expression in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs12mu7fJ&md5=37cf9986d4adc80776bbbc0844b11edcCAS | 23135603PubMed |

Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends in Plant Science 17, 260–270.
Evolution of jasmonate and salicylate signal crosstalk.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xltl2ktbk%3D&md5=4ff59dd3577ca0d180c991f77b014945CAS | 22498450PubMed |

Wu J, Wang L, Wunsche H, Baldwin IT (2013) Narboh D, a respiratory burst oxidase homolog in Nicotiana attenuata, is required for late defense responses after herbivore attack. Journal of Integrative Plant Biology 55, 187–198.
Narboh D, a respiratory burst oxidase homolog in Nicotiana attenuata, is required for late defense responses after herbivore attack.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvFWmsrY%3D&md5=b4ab7a89cd8d3a19c0aa3ad8a328bc50CAS | 23116134PubMed |

Yang ZH (2007) PAML 4: Phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24, 1586–1591.
PAML 4: Phylogenetic analysis by maximum likelihood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGrs7c%3D&md5=486b6bd9bd3ec53781cca12e8aacf714CAS |

Zamora A, Sun Q, Hamblin MT, Aquadro CF, Kresovich S (2009) Positively selected disease response orthologous gene sets in the cereals identified using Sorghum bicolor L. Moench expression profiles and comparative genomics. Molecular Biology and Evolution 26, 2015–2030.
Positively selected disease response orthologous gene sets in the cereals identified using Sorghum bicolor L. Moench expression profiles and comparative genomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVWhs73I&md5=08a2229da067a83830ee79ad44539254CAS | 19506000PubMed |

Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9, 40
I-TASSER server for protein 3D structure prediction.Crossref | GoogleScholarGoogle Scholar | 18215316PubMed |

Zhang ZJ, Chen JM, Su YY, Liu HM, Chen Y, Luo PG, Du XG, Wang D, Zhang HY (2015) TaLHY, a 1R-MYB transcription factor, plays an important role in disease resistance against stripe rust fungus and ear heading in wheat. PLoS One 10, e0127723
TaLHY, a 1R-MYB transcription factor, plays an important role in disease resistance against stripe rust fungus and ear heading in wheat.Crossref | GoogleScholarGoogle Scholar |

Zwicki DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD thesis, School of Biological Sciences, University of Texas-Austin.