Genome-wide association study reveals a set of genes associated with resistance to the Mediterranean corn borer (Sesamia nonagrioides L.) in a maize diversity panel

BMC Plant Biology

Volumn 15, Issue 1, 2015, Pages

  Samayoa, Luis Fernando ^a   Malvar, Rosa Ana ^a   Olukolu, Bode A ^b   Holland, James B ^b,c   Butrón, Ana ^a  

^a MISIÓN BIOLÓGICA DE GALICIA CSIC   (Spain)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Candidate genes; Corn borer; Genome wide association study; Insect resistance; Maize; Mixed linear models; Sesamia nonagrioides

Indexed keywords

ANIMAL; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MAIZE; MOTH; PARASITOLOGY; PHYSIOLOGY; PLANT GENE; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; GENES, PLANT; GENOME-WIDE ASSOCIATION STUDY; MOTHS; POLYMORPHISM, SINGLE NUCLEOTIDE; ZEA MAYS;

EID: 84924054437     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-014-0403-3     Document Type: Article

References (150)

1. Meihls LN, Kaur H, Jander G. Natural variation in maize defense against insect herbivores. Cold Spring Harb Sym. 2012;77:269-83.
2. Malvar RA, Cartea ME, Revilla P, Ordás A, Alvarez A, Mansilla JP. Sources of resistance to pink stem borer and European corn borer in maize. Maydica. 1993;38:313-9.
3. Avantaggiato G, Quaranta F, Desiderio E, Visconti A. Fumonisin contamination of maize hybrids visibly damaged by Sesamia. J Sci Food Agric. 2002;83:13-8.
4. Visconti A, Marasas WFO, Miller JD, Riley R. Mycotoxins of growing interest: Fumonisins. In: Book Mycotoxins of growing interest: Fumonisins. 1999. p. 1-22.
5. Cordero A, Malvar RA, Butrón A, Revilla P, Velasco P, Ordás A. Population dynamics and life-cycle of corn borers in South Atlantic European Coast. Maydica. 1998;43:5-12.
6. Velasco P, Revilla P, Monetti L, Butrón A, Ordás A, Malvar RA. Corn borers (Lepidoptera: Noctuidae; Crambidae) northwestern Spain: population dinamics and distribution. Maydica. 2007;52:195-203.
7. Meissle M, Romeis J, Bigler F. Bt maize and integrated pest management - a European perspective. Pest Manag Sci. 2011;67:1049-58.
8. Speiser B, Tamm L. Regulation of plant protection in organic farming. In: Ehlers R-U, editor. Regulation of Biological Control Agents. Kiel, Germany: Springer; 2011. p. 113-25.
9. Campagne P, Kruger M, Pasquet R, Le Ru B, Van den Berg J. Dominant inheritance of field-evolved resistance to Bt corn in Busseola fusca. PLoS One. 2013;8:e69675.
10. Tabashnik BE, Brévault T, Carrière Y. Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol. 2013;31:510-21.
11. González-Cabrera J, García M, Hernández-Crespo P, Farinós GP, Ortego F, Castañera P. Resistance to Bt maize in Mythimna unipuncta (Lepidoptera: Noctuidae) is mediated by alteration in Cry1Ab protein activation. Insect Biochem Mol Biol. 2013;43:635-43.
12. Gould F. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu Rev Entomol. 1998;43:701-26.
13. Butrón A, Malvar R, Velasco P, Vales M, Ordás A. Combining abilities for maize stem antibiosis, yield loss, and yield under infestation and non infestation with pink stem borer. Crop Sci. 1999;39:691-6.
14. Cartea ME, Malvar RA, Butrón A, Vales MI, Ordás A. Inheritance of antibiosis to Sesamia nonagrioides (Lepidoptera: Noctuidae) in maize. J Econ Entomol. 1999;92:994-8.
15. Papst C, Bohn M, Utz HF, Melchinger AE, Klein D, Eder J. QTL mapping for European corn borer resistance (Ostrinia nubilalis Hb.), agronomic and forage quality traits of testcross progenies in early- maturing European maize (Zea mays L.) germplasm. Theor Appl Genet. 2004;108:1545-54.
16. Schön CC, Lee M, Melchinger AE, Guthrie WD, Woodman WL. Mapping and characterization of quantitative trait loci affecting resistancie against second-generation European corn borer in maize with the aid of RFLPs. Heredity. 1993;70:648-59.
17. Cardinal AJ, Lee M, Sharopova N, Woodman WL, Long MJ. Genetic mapping and analysis of quantitative trait loci for resistance to stalk tunneling by European corn borer in maize. Crop Sci. 2001;41:835-45.
18. Ordás B, Malvar RA, Santiago R, Sandoya G, Romay MC, Butrón A. Mapping of QTL for resistance to the Mediterranean corn borer attack using the intermated B73 × Mo17 (IBM) population in maize. Theor Appl Genet. 2009;119:1451-9.
19. Klenke J, Russel W, Guthrie W. Recurrent selection for resistance to European corn borer in a corn synthetic and correlated effects on agronomic traits. Crop Sci. 1986;26:864-8.
20. Bosque-Pérez N, Kling J, Odubiyi S. Recent advances in the development of sources of resistance to pink stalk borer and African sugarcane borer. In: Insect resistant maize: Recent advances and utilization Proc of an International Symposium. 1997. p. 234-40.
21. Sandoya G, Butrón A, Alvarez A, Ordás A, Malvar RA. Direct response of a maize synthetic to recurrent selection for resistance to stem borers. Crop Sci. 2008;48:113-8.
22. Butrón A, Romay MC, Peña-Asin J, Alvarez A, Malvar RA. Genetic relationship between maize resistance to corn borer attack and yield. Crop Sci. 2012;52:1176-80.
23. Ordás B, Butrón A, Alvarez A, Revilla P, Malvar R. Comparison of two methods of reciprocal recurrent selection in maize (Zea mays L.). Theor Appl Genet. 2012;124:1183-91.
24. Malvar RA, Butrón A, Revilla P, Ordás A. Resistance to the pink stem borer, Sesamia nonagrioides, in maize. Recent Res Devel Plant Sci. 2004;2:1-32.
25. Cartea ME, Malvar RA, Vales I, Butrón A, Ordás A. Inheritance of resistance to ear damage caused by Sesamia nonagrioides (Lepidoptera: Noctuidae) in maize. J Econ Entomol. 2001;94:277-83.
26. Hudon M, Chiang MS. Evaluation of resistance of maize germplasm to the univoltine European corn borer Ostrinia nubilalis (Hübner) and relationship with maize maturity in Quebec. Maydica. 1991;36:69-74.
27. Guthrie W, Russell W. Breeding methodologies and genetic basis of resistance in maize to the European corn borer. In: International Symposium on Methodologies for Developing Host Plant Resistance to Maize Insects Mexico, DF (Mexico) 9-14 Mar 1987. 1989.
28. Krakowsky MD, Brinkman MJ, Woodman WL, Lee M. Genetic components of resistance to stalk tunneling by the European corn borer in maize. Crop Sci. 2002;42:1309-15.
29. Krakowsky MD, Lee M, Holland JB. Genotypic correlation and multivariate QTL analyses for cell wall components and resistance to stalk tunneling by the European corn borer in maize. Crop Sci. 2007;47:485-8.
30. Krakowsky MD, Lee M, Woodman WL, Long MJ, Sharopova N. QTL mapping of resistance to stalk tunneling by the European corn borer in RILs of maize population B73 × De811. Crop Sci. 2004;44:274-82.
31. Orsini E, Krchov L, Uphaus J, Melchinger A. Mapping of QTL for resistance to first and second generation of European corn borer using an integrated SNP and SSR linkage map. Euphytica. 2012;183:197-206.
32. Ordás B, Malvar RA, Santiago R, Butrón A. QTL mapping for Mediterranean corn borer resistance in European flint germplasm using recombinant inbred lines. BMC Genomics. 2010;11:1-10.
33. Bohn M, Khairallah MM, González-de-León D, Hoisington DA, Utz HF, Deutsch JA, et al. QTL mapping in tropical maize: I. Genomic regions affecting leaf feeding resistance to sugarcane borer and other traits. Crop Sci. 1996;36:1352-61.
34. Groh S, González-de-León D, Khairallah MM, Jiang C, Bergvinson D, Bohn M, et al. QTL mapping in tropical maize III. Genomic regions for resistance to Diatraea spp and associated traits in two RIL populations. Crop Sci. 1998;1998:1062-72.
35. Bohn M, Khairallah M, Jiang C, González-de-León D, Hoisington D, Utz H, et al. QTL mapping in tropical maize: II. Comparison of genomic regions for resistance to Diatraea spp. Crop Sci. 1997;37:1892-902.
36. Weiss LA, Arking DE, Daly MJ, Chakravarti A, Brune CW, West K, et al. A genome-wide linkage and association scan reveals novel loci for autism. Nature. 2009;461:802-8.
37. Duerr RH, Taylor KD, Brant SR, Rioux JD, Silverberg MS, Daly MJ, et al. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science. 2006;314:1461-3.
38. Sladek R, Rocheleau G, Rung J, Dina C, Shen L, Serre D, et al. A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature. 2007;445:881-5.
39. Barendse W, Reverter A, Bunch RJ, Harrison BE, Barris W, Thomas MB. A validated whole-genome association study of efficient food conversion in cattle. Genetics. 2007;176:1893-905.
40. Kijas JW, Townley D, Dalrymple BP, Heaton MP, Maddox JF, McGrath A, et al. A genome wide survey of SNP variation reveals the genetic structure of sheep breeds. PLoS One. 2009;4:e4668.
41. Bolormaa S, Hayes B, Savin K, Hawken R, Barendse W, Arthur P, et al. Genome-wide association studies for feedlot and growth traits in cattle. J Anim Sci. 2011;89:1684-97.
42. Fan B, Onteru SK, Du Z-Q, Garrick DJ, Stalder KJ, Rothschild MF. Genome-wide association study identifies loci for body composition and structural soundness traits in pigs. PLoS One. 2011;6:e14726.
43. Tian F, Bradbury PJ, Brown PJ, Hung H, Sun Q, Flint-Garcia S, et al. Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet. 2011;43:159-62.
44. Neumann K, Kobiljski B, Denčić S, Varshney R, Börner A. Genome-wide association mapping: a case study in bread wheat (Triticum aestivum L.). Mol Breed. 2011;27:37-58.
45. Zhu C, Gore M, Buckler ES, Yu J. Status and prospects of association mapping in plants. Plant Genome. 2008;1:5-20.
46. Peiffer JA, Flint-Garcia SA, De Leon N, McMullen MD, Kaeppler SM, Buckler ES. The genetic architecture of maize stalk strength. PLoS One. 2013;8:e67066.
47. Oraguzie NC, Rikkerink EH, Gardiner SE, Silva H. Association mapping in plants. New York: Springer-Verlag GmbH; 2007.
48. Romay MC, Millard MJ, Glaubitz JC, Peiffer J, Swarts K, Casstevens TM, et al. Comprehensive genotyping of the USA national maize inbred seed bank. Genome Biol. 2013;14:1-18.
49. Flint-Garcia SA, Thuillet A-C, Yu J, Pressoir G, Romero SM, Mitchell SE, et al. Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J. 2005;44:1054-64.
50. Liu K, Goodman M, Muse S, Smith JS, Buckler ES, Doebley J. Genetic structure and diversity among maize inbred lines as inferred from DNA microsatellites. Genetics. 2003;165:2117-28.
51. Cook JP, McMullen MD, Holland JB, Tian F, Bradbury P, Ross-Ibarra J, et al. Genetic architecture of maize kernel composition in the nested association mapping and inbred association panels. Plant Physiol. 2012;158:824-34.
52. Olukolu BA, Negeri A, Dhawan R, Venkata B, Sharma P, Garg A, et al. A connected set of genes associated with programmed cell death implicated in controlling the hypersensitive response in maize. Genetics. 2013;193:609-20.
53. Zila CT, Samayoa LF, Santiago R, Butrón A, Holland JB. A genome-wide association study reveals genes associated with fusarium ear rot resistance in a maize core diversity panel. G3-Genes Genomes Genet. 2013;3:2095-104.
54. Atwell S, Huang YS, Vilhjálmsson BJ, Willems G, Horton M, Li Y, et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature. 2010;465:627-31.
55. Chan EK, Rowe HC, Kliebenstein DJ. Understanding the evolution of defense metabolites in Arabidopsis thaliana using genome-wide association mapping. Genetics. 2010;185:991-1007.
56. Ganal MW, Durstewitz G, Polley A, Bérard A, Buckler ES, Charcosset A, et al. A large maize (Zea mays L.) SNP genotyping array: development and germplasm genotyping, and genetic mapping to compare with the B73 reference genome. PLoS One. 2011;6:e28334.
57. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One. 2011;6:e19379.
58. Glaubitz JC, Casstevens TM, Lu F, Harriman J, Elshire RJ, Sun Q, et al. TASSEL-GBS: A High Capacity Genotyping by Sequencing Analysis Pipeline. PLoS One. 2014;9:e90346.
59. Steel RG, Torrie JH. Principles and procedures of statistics. New York, Toronto, London: McGraw-Hill Book Company; 1960.
60. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, et al. The B73 maize genome: complexity, diversity, and dynamics. Science. 2009;326:1112-5.
61. Butrón A, Malvar RA, Velasco P, Cartea ME, Ordás A. Combining abilities and reciprocal effects for maize ear resistance to pink stem borer. Maydica. 1998;43:117-22.
62. Velasco P, Revilla P, Butrón A, Ordás B, Ordás A, Malvar RA. Ear damage of sweet corn inbreds and their hybrids under multiple corn borer infestation. Crop Sci. 2002;42:724-9.
63. Velasco P, Malvar RA, Butrón A, Revilla P, Ordás A. Ear feeding resistance of sweet corn inbreds to pink stem borer. J Am Soc Hortic Sci. 1999;124:268-72.
64. Bohn M, Schulz B, Kreps R, Klein D, Melchinger AE. QTL mapping for resistance against the European corn borer (Ostrinia nubilalis H.) in early maturing European dent germplasm. Theor Appl Genet. 2000;101:907-17.
65. Zhang Z, Ersoz E, Lai C-Q, Todhunter RJ, Tiwari HK, Gore MA, et al. Mixed linear model approach adapted for genome-wide association studies. Nat Genet. 2010;42:355-60.
66. Samayoa LF, Butrón A, Malvar RA. QTL mapping for maize resistance and yield under infestation with Sesamia nonagrioides. Mol Breeding. 2014;34:1331-44.
67. Harper LC, Schaeffer ML, Thistle J, Gardiner J, Andorf C, Campbell D, et al. The MaizeGDB Genome Browser tutorial: one example of database outreach to biologists via video. Database. 2011;2011:1-7.
68. Allan RK, Ratajczak T. Versatile TPR domains accommodate different modes of target protein recognition and function. Cell Stress Chaperones. 2011;16:353-67.
69. Blatch GL, Lässle M. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays. 1999;21:932-9.
70. Pogorelko GV, Mokryakova M, Fursova OV, Abdeeva I, Piruzian ES, Bruskin SA. Characterization of three Arabidopsis thaliana immunophilin genes involved in the plant defense response against P. syringae. Gene. 2014;538:12-22.
71. Hellmann HA, Smeekens S. Sugar sensing and signaling in plants. Front Plant Sci. 2014;5:113.
72. Granot D, David-Schwartz R, Kelly G. Hexose kinases and their role in sugar-sensing and plant development. Front Plant Sci. 2013;4:1-17.
73. Morkunas I, Ratajczak L. The role of sugar signaling in plant defense responses against fungal pathogens. Acta Physiol Plant. 2014;8:409-14.
74. Lee U, Rioflorido I, Hong SW, Larkindale J, Waters ER, Vierling E. The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. Plant J. 2007;49:115-27.
75. Zhong R, Richardson EA, Ye Z-H. The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell. 2007;19:2776-92.
76. Zhong R, Lee C, Zhou J, McCarthy RL, Ye Z-H. A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell. 2008;20:2763-82.
77. Liu Y. Investigation of a KNAT7-BLH-OFP transcription factor complex involved in regulation of secondary cell wall biosynthesis in Arabidopsis thaliana. In: MSc Thesis. Vancouver, Canada: University of British Columbia, Botany; 2010.
78. Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M. The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell. 2005;17:2993-3006.
79. Barros-Rios J, Malvar RA, Jung H-JG, Santiago R. Cell wall composition as a maize defense mechanism against corn borers. Phytochemistry. 2011;72:365-71.
80. Ryan CA. The systemin signaling pathway: differential activation of plant defensive genes. BBA-Protein Struct M. 2000;1477:112-21.
81. Meijer HJ, Munnik T. Phospholipid-based signaling in plants. Annu Rev Plant Biol. 2003;54:265-306.
82. Zhu-Salman K, Bi J-L, Liu T-X. Molecular strategies of plant defense and insect counter-defense. Insect Sci. 2005;12:3-15.
83. Afzal AJ, Wood AJ, Lightfoot DA. Plant receptor-like serine threonine kinases: Roles in signaling and plant defense. Mol Plant-Microbe Interact. 2008;21:507-17.
84. Nürnberger T, Kemmerling B. Receptor protein kinases-pattern recognition receptors in plant immunity. Trends Plant Sci. 2006;11:519-22.
85. Duan Y, Ge C, Liu S, Wang J, Zhou M. A two-component histidine kinase Shk1 controls stress response, sclerotial formation and fungicide resistance in Sclerotinia sclerotiorum. Mol Plant Pathol. 2013;14:708-18.
86. G-i A, Kost C, Boland W. Herbivore-induced, indirect plant defences. BBA-Mol Cell Biol L. 2005;1734:91-111.
87. Engelsdorf T, Hamann T. An update on receptor-like kinase involvement in the maintenance of plant cell wall integrity. Ann Bot. 2014;114:1339-47.
88. Szczegielniak J, Borkiewicz L, Szurmak B, Lewandowska-Gnatowska E, Statkiewicz M, Klimecka M, et al. Maize calcium-dependent protein kinase (ZmCPK11): local and systemic response to wounding, regulation by touch and components of jasmonate signaling. Physiol Plant. 2012;146:1-14.
89. Yang D-H, Hettenhausen C, Baldwin IT, Wu J. Silencing Nicotiana attenuata calcium-dependent protein kinases, CDPK4 and CDPK5, strongly up-regulates wound-and herbivory-induced jasmonic acid accumulations. Plant Physiol. 2012;159:1591-607.
90. Szczegielniak J, Klimecka M, Liwosz A, Ciesielski A, Kaczanowski S, Dobrowolska G, et al. A wound-responsive and phospholipid-regulated maize calcium-dependent protein kinase. Plant Physiol. 2005;139:1970-83.
91. Ma F, Lu R, Liu H, Shi B, Zhang J, Tan M, et al. Nitric oxide-activated calcium/calmodulin-dependent protein kinase regulates the abscisic acid-induced antioxidant defence in maize. J Exp Bot. 2012;63:4835-47.
92. Staiger CJ, Gibbon BC, Kovar DR, Zonia LE. Profilin and actin-depolymerizing factor: modulators of actin organization in plants. Trends Plant Sci. 1997;2:275-81.
93. Tian M, Chaudhry F, Ruzicka DR, Meagher RB, Staiger CJ, Day B. Arabidopsis actin-depolymerizing factor AtADF4 mediates defense signal transduction triggered by the Pseudomonas syringae effector AvrPphB. Plant Physiol. 2009;150:815-24.
94. Henty-Ridilla JL, Li J, Day B, Staiger CJ. Actin depolymerizing factor4 regulates actin dynamics during innate immune signaling in Arabidopsis. Plant Cell. 2014;26:340-52.
95. Porter K, Shimono M, Tian M, Day B. Arabidopsis Actin-Depolymerizing Factor-4 links pathogen perception, defense activation and transcription to cytoskeletal dynamics. PLoS Pathog. 2012;8:e1003006.
96. Wu Y, Zhou JM. Receptor-Like Kinases in Plant Innate Immunity. J Integr Plant Biol. 2013;55:1271-86.
97. Jones DA, Jones J. The role of leucine-rich repeat proteins in plant defences. Adv Bot Res. 1997;24:90-168.
98. McCann MC, Carpita NC. Designing the deconstruction of plant cell walls. Curr Opin Plant Biol. 2008;11:314-20.
99. Zhong R, Demura T, Ye Z-H. SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell. 2006;18:3158-70.
100. Nogueira FT, Schlögl PS, Camargo SR, Fernandez JH. SsNAC23, a member of the NAC domain protein family, is associated with cold, herbivory and water stress in sugarcane. Plant Sci. 2005;169:93-106.
101. Abe M, Abe K, Kuroda M, Arai S. Corn kernel cysteine proteinase inhibitor as a novel cystatin superfamily member of plant origin. Eur J Biochem. 1992;209:933-7.
102. McMullen MD, Frey M, Degenhardt J. Genetics and biochemistry of insect resistance in maize. In: Bennetzen JL, Hake SC, editors. Handbook of maize: Its biology. NY, USA: Springer; 2009. p. 271-89.
103. Ussuf K, Laxmi N, Mitra R. Proteinase inhibitors: plant-derived genes of insecticidal protein for developing insect-resistant transgenic plants. Curr Sci India. 2001;80:847-53.
104. Fabrick J, Behnke C, Czapla T, Bala K, Rao A, Kramer K, et al. Effects of a potato cysteine proteinase inhibitor on midgut proteolytic enzyme activity and growth of the southern corn rootworm, Diabrotica undecimpunctata howardi (Coleoptera: Chrysomelidae). Insect Biochem Mol Biol. 2002;32:405-15.
105. Zhang H, Hedhili S, Montiel G, Zhang Y, Chatel G, Pré M, et al. The basic helix-loop-helix transcription factor CrMYC2 controls the jasmonate-responsive expression of the ORCA genes that regulate alkaloid biosynthesis in Catharanthus roseus. Plant J. 2011;67:61-71.
106. Niu Y, Figueroa P. Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis. J Exp Bot. 2011;62:2143-54.
107. Sasaki-Sekimoto Y, Jikumaru Y, Obayashi T, Saito H, Masuda S, Kamiya Y, et al. Basic Helix-Loop-Helix transcription factors JASMONATE-ASSOCIATED MYC2-LIKE1 (JAM1), JAM2, and JAM3 are negative regulators of jasmonate responses in Arabidopsis. Plant Physiol. 2013;163:291-304.
108. Qi T, Huang H, Wu D, Yan J, Qi Y, Song S, et al. Arabidopsis DELLA and JAZ Proteins Bind the WD-Repeat/bHLH/MYB Complex to Modulate Gibberellin and Jasmonate Signaling Synergy. Plant Cell. 2014;26:1118-33.
109. Song S, Qi T, Fan M, Zhang X, Gao H, Huang H, et al. The bHLH subgroup IIId factors negatively regulate jasmonate-mediated plant defense and development. PLoS Genet. 2013;9:e1003653.
110. Xia H, Yandeau-Nelson M, Thompson DB, Guiltinan MJ. Deficiency of maize starch-branching enzyme i results in altered starch fine structure, decreased digestibility and reduced coleoptile growth during germination. BMC Plant Biol. 2011;11:1-13.
111. Dunwell JM, Gibbings JG, Mahmood T, Saqlan Naqvi S. Germin and germin-like proteins: evolution, structure, and function. Crit Rev Plant Sci. 2008;27:342-75.
112. Davidson RM, Reeves PA, Manosalva PM, Leach JE. Germins: A diverse protein family important for crop improvement. Plant Sci. 2009;177:499-510.
113. Breen J, Bellgard M. Germin-like proteins (GLPs) in cereal genomes: gene clustering and dynamic roles in plant defence. Funct Integr Genomics. 2010;10:463-76.
114. Armstrong JS, Abdel-Mageed H, Fokar M, Allen R, Adamczyk Jr JJ. Dietary effects of cotton tissue expressing germin like protein on beet armyworm (Lepidoptera: Noctuidae) growth, survival and pupation. Fla Entomol. 2013;96:693-700.
115. Ryser U, Schorderet M, Guyot R, Keller B. A new structural element containing glycine-rich proteins and rhamnogalacturonan I in the protoxylem of seed plants. J Cell Sci. 2004;117:1179-90.
116. Ringli C, Keller B, Ryser U. Glycine-rich proteins as structural components of plant cell walls. Cell Mol Life Sci. 2001;58:1430-41.
117. Mangeon A, Junqueira RM, Sachetto-Martins G. Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal Behav. 2010;5:99-104.
118. Showalter AM. Structure and function of plant cell wall proteins. Plant Cell. 1993;5:9.
119. Sturm A. A wound-inducible glycine-rich protein from Daucus carota with homology to single-stranded nucleic acid-binding proteins. Plant Physiol. 1992;99:1689-92.
120. Bohlmann H, Broekaert W. The role of thionins in plant protection. Crit Rev Plant Sci. 1994;13:1-16.
121. De Coninck B, Cammue B, Thevissen K. Modes of antifungal action and in planta functions of plant defensins and defensin-like peptides. Fungal Biol Rev. 2013;26:109-20.
122. Shiau Y-S, Horng S-B, Chen C-S, Huang P-T, Lin C, Hsueh Y-C, et al. Structural analysis of the unique insecticidal activity of novel mungbean defensin VrD1 reveals possibility of homoplasy evolution between plant defensins and scorpion neurotoxins. J Mol Recognit. 2006;19:441-50.
123. Bohlmann H, Apel K. Thionins. Annu Rev Plant Biol. 1991;42:227-40.
124. Kessler A, Baldwin IT. Plant responses to insect herbivory: The emerging molecular analysis. Annu Rev Plant Biol. 2002;53:299-328.
125. Hershko A, Ciechanover A. The ubiquitin system for protein degradation. Annu Rev Biochem. 1992;61:761-807.
126. Zeng L-R, Vega-Sánchez ME, Zhu T, Wang G-L. Ubiquitination-mediated protein degradation and modification: an emerging theme in plant-microbe interactions. Cell Res. 2006;16:413-26.
127. Kelley DR, Estelle M. Ubiquitin-mediated control of plant hormone signaling. Plant Physiol. 2012;160:47-55.
128. Santner A, Estelle M. The ubiquitin-proteasome system regulates plant hormone signaling. Plant J. 2010;61:1029-40.
129. Igarashi D, Tsuda K, Katagiri F. The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J. 2012;71:194-204.
130. Rodriguez PA. Analysis of AtPSKR1, an LRR receptor protein kinase, and other PSK-signalling components in plant defence responses. In: PhD Thesis. Tübingen, Germany: University of Tübingen, Mathematics and Natural Sciences; 2011.
131. Angelini R, Tisi A, Rea G, Chen MM, Botta M, Federico R, et al. Involvement of polyamine oxidase in wound healing. Plant Physiol. 2008;146:162-77.
132. Wimalasekera R, Tebartz F, Scherer GF. Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci. 2011;181:593-603.
133. Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Barr JE, Rodermel S, et al. Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J. 2002;32:329-42.
134. Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, et al. Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J. 1997;16:4806-16.
135. Kaur R, Gupta AK, Taggar GK. Role of catalase, H2O2 and phenolics in resistance of pigeonpea towards Helicoverpa armigera (Hubner). Acta Physiol Plant. 2014;36:1513-27.
136. Bajsa J, Pan Z, Duke SO. Serine/threonine protein phosphatases: Multi-purpose enzymes in control of defense mechanisms. Plant Signal Behav. 2011;6:1921.
137. Vyroubalová Š, Václavíková K, Turečková V, Novák O, Šmehilová M, Hluska T, et al. Characterization of new maize genes putatively involved in cytokinin metabolism and their expression during osmotic stress in relation to cytokinin levels. Plant Physiol. 2009;151:433-47.
138. Smigocki A, Neal Jr J, McCanna I, Douglass L. Cytokinin-mediated insect resistance in Nicotiana plants transformed with the ipt gene. Plant Mol Biol. 1993;23:325-35.
139. Giron D, Frago E, Glevarec G, Pieterse CM, Dicke M. Cytokinins as key regulators in plant-microbe-insect interactions: connecting plant growth and defence. Funct Ecol. 2013;27:599-609.
140. De Los CG, Gianola D, Allison DB. Predicting genetic predisposition in humans: the promise of whole-genome markers. Nat Rev Genet. 2010;11:880-6.
141. Flint-Garcia SA, Darrah LL, McMullen MD, Hibbard BE. Phenotypic versus marker-assisted selection for stalk strength and second-generation European corn borer resistance in maize. Theor Appl Genet. 2003;107:1331-6.
142. Eizaguirre M, Albajes R. Diapause induction in the stem corn borer Sesamia nonagrioides (Lepidoptera, Noctuidae). Entomol Gen. 1992;17:277-83.
143. SAS Institute Inc. SAS 9.3 Guide to software updates. Cary, NC, USA, SAS Institute Inc. 2011; 314 p
144. Holland JB, Nyquist WE, Cervantes-Martínez CT. Estimated an interpreting heritability for plant breeding: An update. In: Janick J, editor. Plant Breeding Reviews, vol. Volume 22. Hoboken, New Jersey, USA: Jonh Wiley & Sons; 2003. p. 9-112.
145. Holland JB. Estimating genotypic correlations and their standard errors using multivariate restricted maximum likelihood estimation with SAS Proc MIXED. Crop Sci. 2006;46:642-56.
146. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics. 2007;23:2633-5.
147. Yu J, Pressoir G, Briggs WH, Vroh I, Yamasaki I, Doebley JF, et al. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet. 2006;38:203-8.
148. Valdar W, Holmes CC, Mott R, Flint J. Mapping in structured populations by resample model averaging. Genetics. 2009;182:1263-77.
149. Panagiotou OA, Ioannidis JP. What should the genome-wide significance threshold be? Empirical replication of borderline genetic associations. Int J Epidemiol. 2012;41:273-86.
150. R Core Team. R: A languange and environment for statistical computing. In: Book R: A languange and environment for statistical computing (Editor ed.^eds.). Vienna, Austria: City: R Foundation for Statistical Computing; 2013.