Metabolic and enzymatic changes associated with carbon mobilization, utilization and replenishment triggered in grain amaranth (Amaranthus cruentus) in response to partial defoliation by mechanical injury or insect herbivory

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Castrillón Arbeláez, Paula A ^a   Martínez Gallardo, Norma ^a   Arnaut, Hamlet A ^a,b   Tiessen, Axel ^a   Délano Frier, John P ^a  

^a Unidad de Biotecnología e Ingeniería Genética de Plantas Cinvestav Irapuato   (Mexico)

^b UNIVERSIDAD AUTÓNOMA DE NUEVO LEÓN   (Mexico)

Author keywords

Carbohydrate metabolism; Carbohydrate mobilization; Carbon sequestration; Defoliation; Grain amaranth; Plasticity; Tolerance

Indexed keywords

AMARANTHUS; AMARANTHUS CAUDATUS; AMARANTHUS CRUENTUS; AMARANTHUS HYPOCHONDRIACUS; HEXAPODA;

BETA FRUCTOFURANOSIDASE; CARBON; CYCLOPENTANE DERIVATIVE; FRUCTOSE; GLUCOSE; GLUCOSYLTRANSFERASE; JASMONIC ACID; MESSENGER RNA; OXYLIPIN; STARCH; SUCROSE; SUCROSE SYNTHASE; VEGETABLE PROTEIN;

AMARANTHUS; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CARBOHYDRATE METABOLISM; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HERBIVORY; INSECT; MECHANICAL STRESS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PHYSIOLOGY; PLANT GENE; PLANT LEAF; PLANT ROOT; PLANT SEED; PLANT STEM;

AMARANTHUS; AMINO ACID SEQUENCE; ANIMALS; BETA-FRUCTOFURANOSIDASE; CARBOHYDRATE METABOLISM; CARBON; CLONING, MOLECULAR; CYCLOPENTANES; FRUCTOSE; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLUCOSE; GLUCOSYLTRANSFERASES; HERBIVORY; INSECTS; MOLECULAR SEQUENCE DATA; OXYLIPINS; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANT STEMS; RNA, MESSENGER; SEEDS; STARCH; STRESS, MECHANICAL; SUCROSE;

EID: 84872369537     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-163     Document Type: Article

References (121)

1. Flowers TJ, Colmer TD. Salinity tolerance in halophytes. New Phytol 2008, 179:945-963. 10.1111/j.1469-8137.2008.02531.x, 18565144.
2. Akubugwo IE, Obasi NA, Chinyere GC, Ugbogu AE. Nutritional and chemical value of Amaranthus hybridus L. leaves from Afikpo, Nigeria. Afr J Biotechnol 2007, 6:2833-2839.
3. Brenner D, Baltensperger D, Kulakow P, Lehmann J, Myers R, Slabbert M, Sleugh B. Genetic resources and breeding of Amaranthus. Plant Breed Rev 2000, 19:227-285.
4. Huerta-Ocampo J, Barba de la Rosa A. Amaranth: a pseudo-cereal with nutraceutical properties. Curr Nutr Food Sci 2011, 7:1-9.
5. Johnson BL, Henderson TL. Water use patterns of grain amaranth in the northern Great Plains. Agron J 2002, 94:1437-1443.
6. Omami EN, Hammes PS, Robbertse PJ. Differences in salinity tolerance for growth and water-use efficiency in some amaranth (Amaranthus spp.) genotypes. New Zeal J Crop Hort 2006, 34:11-22.
7. Aragón-García A, Huato MAD, Lara MH, Sáenz-de-Cabezón F, Pérez-Moreno I, Marco-Mancebón V, López-Olguín JF. Insect occurrence and losses due to phytophagous species in the amaranth Amaranthus hypocondriacus L. crop in Puebla, Mexico. Afr J Agr Res 2011, 6:5924-5929.
8. Délano-Frier JP, Martínez-Gallardo NA, Martínez-de la Verga O, Salas-Araiza MD, Barbosa-Jaramillo ER, Torres A, Vargas P, Borodanenko A. The effect of exogenous jasmonic acid on induced resistance and productivity in amaranth (Amaranthus hypochondriacus) is influenced by environmental conditions. J Chem Ecol 2004, 30:1001-1034.
9. Gassmann AJ. Effect of photosynthetic efficiency and water availability on tolerance of leaf removal in Amaranthus hybridus. J Ecol 2004, 92:882-892.
10. Weaver SE, Mcwilliams EL. The biology of Canadian weeds .44. Amaranthus retroflexus L., A. powellii S. Wats and A. hybridus L. Can J Plant Sci 1980, 60:1215-1234.
11. Grubben GJH. The cultivation of amaranth as a tropical leaf vegetable with special reference to South Dahomey 1976, Amsterdam: Department of Agricultural Research, Royal Tropical Institute.
12. Espitia-Rangel E, Mapes-Sánchez C, Escobedo-López D, de la O-Olán M, Rivas-Valencia P, Martínez-Trejo G, Cortés-Espinosa L, Hernández-Casillas JM. Conservación y uso de los recursos genéticos de amaranto en México 2010, Celaya, Guanajuato, México: SINAREFI-INIFAP-UNAM, Centro de Investigación Regional Centro.
13. Weber LE, Irwin MD, Baltensperger DD, Applegate WW, Lehmann JW, Putnam DH. Amaranth-grain production guide 1990, Emmaus, PA: Rodale Press.
14. Wilson RL. Studies of insects feeding on grain amaranth in the Midwest. J Kansas Entomol Soc 1989, 62:440-448.
15. Fomsgaard I, Añon M, Barba de la Rosa A, Christophersen C, Dusek K, Délano- Frier J, Espinoza Pérez J, Fonseca A, Janovská D, Kudsk P, Labouriau R, Lacayo-Romero M, Martínez N, Matus F, Matusová K, Mathiassen S, Noellemeyer E, Pedersen H, Stavelikova H, Steffensen S, de Troiani R, Taberner A. Adding Value to Holy Grain: Providing the Key Tools for the Exploitation of Amaranth - the Protein-rich Grain of the Aztecs. Results from a Joint European - Latin American Research Project 2010, Denmark: Department of Integrated Pest Management, Aarhus University, Faculty of Agricultural Sciences.
16. Vargas-Ortiz E. Estudio de la redistribución de carbohidratos y nitrógeno como posible mecanismo de tolerancia a pérdida de tejido foliar por herbivoría y/o daño mecánico en amaranto. MSc thesis 2009, Cinvestav-Unidad Irapuato, Departamento de Biotecnología y Bioquímica.
17. Martínez-Moreno D, Nuñez-Farfán J, Terrazas T, Muiz LD, Trinidad-Santos A, Trejo C, Larque-Saavedra A. Plastic responses to clipping in two species of Amaranthus from the Sierra Norte de Puebla, Mexico. Genet Resour Crop Ev 1999, 46:225-234.
18. Bruce TJ, Pickett JA. Plant defence signalling induced by biotic attacks. Curr Opin Plant Biol 2007, 10:387-392. 10.1016/j.pbi.2007.05.002, 17627867.
19. Howe GA, Jander G. Plant immunity to insect herbivores. Annu Rev Plant Biol 2008, 59:41-66. 10.1146/annurev.arplant.59.032607.092825, 18031220.
20. Nuñez-Farfán J, Fornoni J, Valverde PL. The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol S 2007, 38:541-566.
21. Schwachtje J, Baldwin IT. Why does herbivore attack reconfigure primary metabolism?. Plant Physiol 2008, 146:845-851. 10.1104/pp.107.112490, 2259057, 18316639.
22. Stowe KA, Marquis RJ, Hochwender CG, Simms EL. The evolutionary ecology of tolerance to consumer damage. Annu Rev Ecol Syst 2000, 31:565-595.
23. Farrar JF. Sink strength: what is it and how do we measure it?. Plant Cell Environ 1993, 16:1015.
24. McCormick AJ, Cramer MD, Watt DA. Sink strength regulates photosynthesis in sugarcane. New Phytol 2006, 171:759-770. 10.1111/j.1469-8137.2006.01785.x, 16918547.
25. Paul MJ, Pellny TK. Carbon metabolite feedback regulation of leaf photosynthesis and development. J Exp Bot 2003, 54:539-547. 10.1093/jxb/erg052, 12508065.
26. Rolland F, Baena-Gonzalez E, Sheen J. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Physiol 2006, 57:675-709.
27. McCormick AJ, Cramer MD, Watt DA. Changes in photosynthetic rates and gene expression of leaves during a source-sink perturbation in sugarcane. Ann Bot 2008, 101:89-102. 2701831, 17942591.
28. Baldwin IT. Herbivory simulations in ecological research. Trends Ecol Evol 1990, 5:91-93. 10.1016/0169-5347(90)90237-8, 21232330.
29. Lethilä K, Bolt E. The use and usefulness of artificial herbivory in plant-herbivore studies. Ecological Studies 2004, 257-273. Berlin Heidelberg: Springer-Verlag, Wiesser WW SE.
30. Délano-Frier JP, Avilés-Arnaut H, Casarrubias-Castillo K, Casique-Arroyo G, Castrillón-Arbeláez PA, Herrera-Estrella L, Massange-Sánchez J, Martínez-Gallardo NA, Parra-Cota FI, Vargas-Ortiz E, Estrada-Hernández MG. Transcriptomic analysis of grain amaranth (Amaranthus hypochondriacus) using 454 pyrosequencing: comparison with A. tuberculatus, expression profiling in stems and in response to biotic and abiotic stress. BMC Genomics 2011, 12:363. 10.1186/1471-2164-12-363, 3146458, 21752295.
31. Klotz KL, Haagenson DM. Wounding, anoxia and cold induce sugarbeet sucrose synthase transcriptional changes that are unrelated to protein expression and activity. J Plant Physiol 2008, 165:423-434. 10.1016/j.jplph.2007.02.001, 17395334.
32. Vargas WA, Pontis HG, Salerno GL. Differential expression of alkaline and neutral invertases in response to environmental stresses: characterization of an alkaline isoform as a stress-response enzyme in wheat leaves. Planta 2007, 226:1535-1545. 10.1007/s00425-007-0590-3, 17674033.
33. Xiang L, Le Roy K, Bolouri-Moghaddam MR, Vanhaecke M, Lammens W, Rolland F, Van den Ende W. Exploring the neutral invertase-oxidative stress defence connection in Arabidopsis thaliana. J Exp Bot 2011, 62:3849-3862. 10.1093/jxb/err069, 3134342, 21441406.
34. Gonzalez MC, Roitsch T, Cejudo FJ. Circadian and developmental regulation of vacuolar invertase expression in petioles of sugar beet plants. Planta 2005, 222:386-395. 10.1007/s00425-005-1542-4, 16052318.
35. Ohyama A, Nishimura S, Hirai M. Cloning of cDNA for a cell wall-bound acid invertase from tomato (Lycopersicon esculentum) and expression of soluble and cell wall-bound invertases in plants and wounded leaves of L. esculentum and L. peruvianum. Genes Genet Syst 1998, 73:149-157. 10.1266/ggs.73.149, 9794080.
36. Yin YG, Kobayashi Y, Sanuki A, Kondo S, Fukuda N, Ezura H, Sugaya S, Matsukura C. Salinity induces carbohydrate accumulation and sugar-regulated starch biosynthetic genes in tomato (Solanum lycopersicum L. cv. 'Micro-Tom') fruits in an ABA- and osmotic stress-independent manner. J Exp Bot 2010, 61:563-574. 10.1093/jxb/erp333, 2803223, 19995825.
37. Kwak MS, Min SR, Lee SM, Kim KN, Liu JR, Paek KH, Shin JS, Bae JM. A sepal-expressed ADP-glucose pyrophosphorylase gene (NtAGP) is required for petal expansion growth in 'Xanthi' tobacco. Plant Physiol 2007, 145:277-289. 10.1104/pp.107.102095, 1976561, 17660352.
38. Adhikari TB, Balaji B, Breeden J, Goodwin SB. Resistance of wheat to Mycosphaerella graminicola involves early and late peaks of gene expression. Physiol Mol Plant P 2007, 71:55-68.
39. Weigelt K, Kuster H, Rutten T, Fait A, Fernie AR, Miersch O, Wasternack C, Emery RJ, Desel C, Hosein F, Muller M, Saalbach I, Weber H. ADP-glucose pyrophosphorylase-deficient pea embryos reveal specific transcriptional and metabolic changes of carbon-nitrogen metabolism and stress responses. Plant Physiol 2009, 149:395-411. 10.1104/pp.108.129940, 2613696, 18987213.
40. Rausch T, Greiner S. Plant protein inhibitors of invertases. Biochim Biophys Acta 2004, 1696:253-261. 10.1016/j.bbapap.2003.09.017, 14871666.
41. Castrillón-Arbeláez PA, Délano-Frier JP. The sweet side of inhibition: invertase inhibitors and their importance in plant development and stress responses. Curr Enz Inhib 2011, 7:169-177.
42. Sturm A, Chrispeels MJ. cDNA cloning of carrot extracellular beta-fructosidase and its expression in response to wounding and bacterial-infection. Plant Cell 1990, 2:1107-1119. 159958, 2152110.
43. Downie SR, Katz-Downie DS, Cho KJ. Relationships in the caryophyllales as suggested by phylogenetic analyses of partial chloroplast DNA ORF2280 homolog sequences. Am J Bot 1997, 84:253-273. 10.2307/2446087, 21712205.
44. Ray T, Roy SC. Phylogenetic relationships between members of Amaranthaceae and Chenopodiaceae of lower Gangetic plains using RAPD and ISSR markers. Bangladesh J Bot 2007, 36:21-28.
45. Nakata PA, Anderson JM, Okita TW. Structure and expression of the potato ADP-glucose pyrophosphorylase small subunit. J Biol Chem 1994, 269:30798-30807.
46. Müller-Rober B, Nast G, Willmitzer L. Isolation and expression analysis of cDNA clones encoding a small and a large subunit of ADP-glucose pyrophosphorylase from sugar beet. Plant Mol Biol 1995, 27:191-197. 10.1007/BF00019190, 7865789.
47. Bieniawska Z, Barratt DHP, Garlick AP, Thole V, Kruger NJ, Martin C, Zrenner R, Smith AM. Analysis of the sucrose synthase gene family in Arabidopsis. Plant J 2007, 49:810-828. 10.1111/j.1365-313X.2006.03011.x, 17257168.
48. Godt DE, Riegel A, Roitsch T. Regulation of sucrose synthase expression in Chenopodium rubrum: characterization of sugar induced expression in photoautotrophic suspension cultures and sink tissue specific expression in plants. J Plant Physiol 1995, 146:231-238.
49. Haagenson DM, Klotz KL, McGrath JM. Sugarbeet sucrose synthase genes differ in organ-specific and developmental expression. J Plant Physiol 2006, 163:102-106. 10.1016/j.jplph.2005.05.006, 16360809.
50. Komatsu A, Moriguchi T, Koyama K, Omura M, Akihama T. Analysis of sucrose synthase genes in citrus suggests different roles and phylogenetic relationships. J Exp Bot 2002, 53:61-71. 10.1093/jexbot/53.366.61, 11741042.
51. Hesse H, Willmitzer L. Expression analysis of a sucrose synthase gene from sugar beet (Beta vulgaris L.). Plant Mol Biol 1996, 30:863-872. 10.1007/BF00020799, 8639746.
52. Subbaiah CC, Palaniappan A, Duncan K, Rhoads DM, Huber SC, Sachs MM. Mitochondrial localization and putative signaling function of sucrose synthase in maize. J Biol Chem 2006, 281:15625-15635. 10.1074/jbc.M600355200, 16606624.
53. Sturm A, Hess D, Lee HS, Lienhard S. Neutral invertase is a novel type of sucrose-cleaving enzyme. Physiol Plant 1999, 107:159-165.
54. Vargas WA, Pontis HG, Salerno GL. New insights on sucrose metabolism: evidence for an active A/N-Inv in chloroplasts uncovers a novel component of the intracellular carbon trafficking. Planta 2008, 227:795-807. 10.1007/s00425-007-0657-1, 18034262.
55. Nonis A, Ruperti B, Pierasco A, Canaguier A, Adam-Blondon AF, Di Gaspero G, Vizzotto G. Neutral invertases in grapevine and comparative analysis with Arabidopsis, poplar and rice. Planta 2008, 229:129-142. 10.1007/s00425-008-0815-0, 18800225.
56. Huang LF, Bocock PN, Davis JM, Koch KE. Regulation of invertase: a suite of transcriptional and post-transcriptional mechanisms. Funct Plant Biol 2007, 34:499-507.
57. Rae AL, Casu RE, Perroux JM, Jackson MA, Grof CPL. A soluble acid invertase is directed to the vacuole by a signal anchor mechanism. J Plant Physiol 2011, 168:983-989. 10.1016/j.jplph.2010.11.003, 21156329.
58. Maas C, Laufs J, Grant S, Korfhage C, Werr W. The combination of a novel stimulatory element in the first exon of the maize Shrunken-1 gene with the following intron 1 enhances reporter gene expression up to 1000-fold. Plant Mol Biol 1991, 16:199-207. 10.1007/BF00020552, 1893097.
59. Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS. Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant 2010, 3:942-955. 10.1093/mp/ssq044, 20729475.
60. Zhu Y, Cai XL, Wang ZY, Hong MM. An interaction between a MYC protein and an EREBP protein is involved in transcriptional regulation of the rice Wx gene. J Biol Chem 2003, 278:47803-47811. 10.1074/jbc.M302806200, 12947109.
61. Alberto F, Bignon C, Sulzenbacher G, Henrissat B, Czjzek M. The three-dimensional structure of invertase (beta-fructosidase) from Thermotoga maritima reveals a bimodular arrangement and an evolutionary relationship between retaining and inverting glycosidases. J Biol Chem 2004, 279:18903-18910. 10.1074/jbc.M313911200, 14973124.
62. Bocock PN, Morse AM, Dervinis C, Davis JM. Evolution and diversity of invertase genes in Populus trichocarpa. Planta 2008, 227:565-576. 10.1007/s00425-007-0639-3, 17938954.
63. Pons T, Olmea O, Chinea G, Beldarrain A, Marquez G, Acosta N, Rodriguez L, Valencia A. Structural model for family 32 of glycosyl-hydrolase enzymes. Proteins 1998, 33:383-395. 10.1002/(SICI)1097-0134(19981115)33:3<383::AID-PROT7>3.0.CO;2-R, 9829697.
64. Huber SC. Relationship between photosynthetic starch formation and dry-weight partitioning between the root and shoot. Can J Bot 1983, 61:2709-2716.
65. Orians CM, Thorn A, Gomez S. Herbivore-induced resource sequestration in plants: why bother?. Oecologia 2011, 167:1-9. 10.1007/s00442-011-1968-2, 21431939.
66. Barry KM, Quentin A, Eyles A, Pinkard EA. Consequences of resource limitation for recovery from repeated defoliation in Eucalyptus globulus Labilladiere. Tree Physiol 2012, 32:24-35. 10.1093/treephys/tpr128, 22174093.
67. Kosola KR, Dickmann DI, Paul EA, Parry D. Repeated insect defoliation effects on growth, nitrogen acquisition, carbohydrates, and root demography of poplars. Oecologia 2001, 129:65-74.
68. Palacio S, Hester AJ, Maestro M, Millard P. Browsed Betula pubescens trees are not carbon-limited. Funct Ecol 2008, 22:808-815.
69. Palacio S, Paterson E, Sim A, Hester AJ, Millard P. Browsing affects intra-ring carbon allocation in species with contrasting wood anatomy. Tree Physiol 2011, 31:150-159. 10.1093/treephys/tpq110, 21388994.
70. Tschaplinski TJ, Blake TJ. Carbohydrate mobilization following shoot defoliation and decapitation in hybrid poplar. Tree Physiol 1994, 14:141-151. 10.1093/treephys/14.2.141, 14967709.
71. Lee JM, Sathish P, Donaghy DJ, Roche JR. Plants modify biological processes to ensure survival following carbon depletion: a Lolium perenne model. PLoS ONE 2010, 5:e12306. 10.1371/journal.pone.0012306, 2924894, 20808836.
72. Caldwell MM, Richards JH, Johnson DA, Nowak RS, Dzurec RS. Coping with herbivory: photosynthetic capacity and resource allocation in two semiarid Agropyron bunchgrasses. Oecologia 1981, 50:14-24.
73. Rivera-Solís G, Abdala-Roberts L, Cervera JC, Parra-Tabla V, Ruiz-Ruiz J, Betancur-Ancona D. Mechanisms and traits associated with compensation for defoliation in Ruellia nudiflora. Plant Ecol 2012, 213:303-314.
74. Fang XW, Li JH, Xiong YC, Xu DH, Fan XW, Li FM. Responses of Caragana korshinskii Kom. to shoot removal: mechanisms underlying regrowth. Ecol Res 2008, 23:863-871.
75. Taliercio EW, Chourey PS. Post-transcriptional control of sucrose synthase expression in anaerobic seedlings of maize. Plant Physiol 1989, 90:1359-1364. 10.1104/pp.90.4.1359, 1061896, 16666936.
76. Barrero-Sicilia C, Hernando-Amado S, Gonzalez-Melendi P, Carbonero P. Structure, expression profile and subcellular localisation of four different sucrose synthase genes from barley. Planta 2011, 234:391-403. 10.1007/s00425-011-1408-x, 21505865.
77. Baud S, Vaultier MN, Rochat C. Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. J Exp Bot 2004, 55:397-409. 10.1093/jxb/erh047, 14739263.
78. Koch K. Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 2004, 7:235-246. 10.1016/j.pbi.2004.03.014, 15134743.
79. Rojo E, Zouhar J, Carter C, Kovaleva V, Raikhel NV. A unique mechanism for protein processing and degradation in Arabidopsis thaliana. Proc Natl Acad Sci USA 2003, 100:7389-7394. 10.1073/pnas.1230987100, 165885, 12773619.
80. Zhang HJ, Dong SM, Wang MF, Wang W, Song WW, Dou XY, Zheng XB, Zhang ZG. The role of vacuolar processing enzyme (VPE) from Nicotiana benthamiana in the elicitor-triggered hypersensitive response and stomatal closure. J Exp Bot 2010, 61:3799-3812. 10.1093/jxb/erq189, 2921209, 20603283.
81. Arnold TM, Schultz JC. Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus. Oecologia 2002, 130:585-593.
82. Roitsch T, Gonzalez MC. Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 2004, 9:606-613. 10.1016/j.tplants.2004.10.009, 15564128.
83. Murayama S, Handa H. Genes for alkaline/neutral invertase in rice: alkaline/neutral invertases are located in plant mitochondria and also in plastids. Planta 2007, 225:1193-1203. 10.1007/s00425-006-0430-x, 17086397.
84. Tetlow IJ, Morell MK, Emes MJ. Recent developments in understanding the regulation of starch metabolism in higher plants. J Exp Bot 2004, 55:2131-2145. 10.1093/jxb/erh248, 15361536.
85. Tiessen A, Hendriks JH, Stitt M, Branscheid A, Gibon Y, Farre EM, Geigenberger P. Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 2002, 14:2191-2213. 10.1105/tpc.003640, 150765, 12215515.
86. Tiessen A, Prescha K, Branscheid A, Palacios N, McKibbin R, Halford NG, Geigenberger P. Evidence that SNF1-related kinase and hexokinase are involved in separate sugar-signalling pathways modulating post-translational redox activation of ADP-glucose pyrophosphorylase in potato tubers. Plant J 2003, 35:490-500. 10.1046/j.1365-313X.2003.01823.x, 12904211.
87. Li J, Ezquer I, Bahaji A, Montero M, Ovecka M, Baroja-Fernandez E, Munoz FJ, Merida A, Almagro G, Hidalgo M, Sesma MT, Pozueta-Romero J. Microbial volatile-induced accumulation of exceptionally high levels of starch in Arabidopsis leaves is a process involving NTRC and starch synthase classes III and IV. Mol Plant Microbe Interact 2011, 24:1165-1178. 10.1094/MPMI-05-11-0112, 21649509.
88. Szydlowski N, Ragel P, Raynaud S, Lucas MM, Roldan I, Montero M, Munoz FJ, Ovecka M, Bahaji A, Planchot V, Pozueta-Romero J, D'Hulst C, Merida A. Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthases. Plant Cell 2009, 21:2443-2457. 10.1105/tpc.109.066522, 2751949, 19666739.
89. Kossmann J, Lloyd J. Understanding and influencing starch biochemistry. Crit Rev Biochem Mol 2000, 35:141-196.
90. Chen S, Li XQ, Zhao A, Wang L, Li X, Shi Q, Chen M, Guo J, Zhang J, Qi D, Liu G. Genes and pathways induced in early response to defoliation in rice seedlings. Curr Issues Mol Biol 2009, 11:81-100.
91. Fang XW, Li YB, Xu DH, Yang XM, Wang G. Activities of starch hydrolytic enzymes and starch mobilization in roots of Caragana korshinskii following above-ground partial shoot removal. Trees-Struct Funct 2007, 21:93-100.
92. Gallagher JA, Volenec JJ, Turner LB, Pollock CJ. Starch hydrolytic enzyme activities following defoliation of white clover. Crop Sci 1997, 37:1812-1818.
93. Schwachtje J, Minchin PEH, Jahnke S, van Dongen JT, Schittko U, Baldwin IT. SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc Natl Acad Sci U S A 2006, 103:12935-12940. 10.1073/pnas.0602316103, 1568949, 16912118.
94. Sauer N. Molecular physiology of higher plant sucrose transporters. FEBS Lett 2007, 581:2309-2317. 10.1016/j.febslet.2007.03.048, 17434165.
95. Berthier A, Desclos M, Amiard V, Morvan-Bertrand A, Demmig-Adams B, Adams WW, Turgeon R, Prud'homme MP, Noiraud-Romy N. Activation of sucrose transport in defoliated Lolium perenne L.: an example of apoplastic phloem loading plasticity. Plant Cell Physiol 2009, 50:1329-1344. 10.1093/pcp/pcp081, 19520670.
96. Meyer S, Lauterbach C, Niedermeier M, Barth I, Sjolund RD, Sauer N. Wounding enhances expression of AtSUC3, a sucrose transporter from Arabidopsis sieve elements and sink tissues. Plant Physiol 2004, 134:684-693. 10.1104/pp.103.033399, 344544, 14739351.
97. Kubis SE, Pike MJ, Everett CJ, Hill LM, Rawsthorne S. The import of phosphoenolpyruvate by plastids from developing embryos of oilseed rape, Brassica napus (L.), and its potential as a substrate for fatty acid synthesis. J Exp Bot 2004, 55:1455-1462. 10.1093/jxb/erh157, 15208349.
98. Prabhakar V, Lottgert T, Geimer S, Dormann P, Kruger S, Vijayakumar V, Schreiber L, Gobel C, Feussner K, Feussner I, Marin K, Staehr P, Bell K, Flugge UI, Hausler RE. Phosphoenolpyruvate provision to plastids is essential for gametophyte and sporophyte development in Arabidopsis thaliana. Plant Cell 2010, 22:2594-2617. 10.1105/tpc.109.073171, 2947176, 20798327.
99. Flugge UI, Hausler RE, Ludewig F, Gierth M. The role of transporters in supplying energy to plant plastids. J Exp Bot 2011, 62:2381-2392. 10.1093/jxb/erq361, 21511915.
100. Sánchez-Hernández C, Martínez-Gallardo N, Guerrero-Rangel A, Valdés-Rodríguez S, Délano-Frier J. Trypsin and a-amylase inhibitors are differentially induced in leaves of amaranth (Amaranthus hypochondriacus) in response to biotic and abiotic stress. Physiol Plant 2004, 122:254-264.
101. Babst BA, Ferrieri RA, Gray DW, Lerdau M, Schlyer DJ, Schueller M, Thorpe MR, Orians CM. Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol 2005, 167:63-72. 10.1111/j.1469-8137.2005.01388.x, 15948830.
102. Baldwin IT. Methyl jasmonate-induced nicotine production in Nicotiana attenuata: inducing defenses in the field without wounding. Entomol Exp Appl 1996, 80:213-220.
103. Thaler JS, Stout MJ, Karban R, Duffey SS. Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J Chem Ecol 1996, 22:1767-1781.
104. Kerchev PI, Fenton B, Foyer CH, Hancock RD. Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant Cell Environ 2012, 35:441-453. 10.1111/j.1365-3040.2011.02399.x, 21752032.
105. Massange-Sánchez J. Análisis de la expresión y caracterización molecular del gen Ah24 inducido por daño mecánico, herbivoría y adición exógena de MeJA en plantas de Amaranthus hypochondriacus. MSc thesis 2011, Cinvestav-Unidad Irapuato, Departamento de Biotecnología y Bioquímica.
106. Babst BA, Ferrieri RA, Thorpe MR, Orians CM. Lymantria dispar herbivory induces rapid changes in carbon transport and partitioning in Populus nigra. Entomol Exp Appl 2008, 128:117-125.
107. Beardmore T, Wetzel S, Kalous M. Interactions of airborne methyl jasmonate with vegetative storage protein gene and protein accumulation and biomass partitioning in Populus plants. Can J Forest Res 2000, 30:1106-1113.
108. Cipollini D. Consequences of the overproduction of methyl jasmonate on seed production, tolerance to defoliation and competitive effect and response of Arabidopsis thaliana. New Phytol 2007, 173:146-153. 10.1111/j.1469-8137.2006.01882.x, 17176401.
109. Halitschke R, Gase K, Hui DQ, Schmidt DD, Baldwin IT. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VI. Microarray analysis reveals that most herbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates. Plant Physiol 2003, 131:1894-1902. 10.1104/pp.102.018184, 166945, 12692348.
110. McCloud ES, Baldwin IT. Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 1997, 203:430-435.
111. Steinbrenner AD, Gomez S, Osorio S, Fernie AR, Orians CM. Herbivore-induced changes in tomato (Solanum lycopersicum) primary metabolism: a whole plant perspective. J Chem Ecol 2011, 37:1294-1303. 10.1007/s10886-011-0042-1, 22161151.
112. Walling LL. The myriad plant responses to herbivores. J Plant Growth Regul 2000, 19:195-216.
113. Gepstein S, Sabehi G, Carp MJ, Hajouj T, Nesher MFO, Yariv I, Dor C, Bassani M. Large-scale identification of leaf senescence-associated genes. Plant J 2003, 36:629-642. 10.1046/j.1365-313X.2003.01908.x, 14617064.
114. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
115. Roitsch T, Bittner M, Godt DE. Induction of apoplastic invertase of Chenopodium rubrum by D-glucose and a glucose analog and tissue-specific expression suggest a role in sink-source regulation. Plant Physiol 1995, 108:285-294. 10.1104/pp.108.1.285, 157333, 7784506.
116. Murray MG, Thompson WF. Rapid isolation of high molecular-weight plant DNA. Nucleic Acids Res 1980, 8:4321-4325. 10.1093/nar/8.19.4321, 324241, 7433111.
117. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
118. Teska JD, Coyne SR, Ezzel LJW, Allan CM, Redus SL. Identification of Bacillus anthracis using gas chromatographic analysis of cellular fatty acids and a commercially available database. Agilent Technologies Inc 2003, 1-5.
119. Wright DP, Scholes JD, Read DJ. Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ 1998, 21:209-216.
120. Scholes JD, Lee PJ, Horton P, Lewis DH. Invertase: understanding changes in the photosynthetic and carbohydrate metabolism of barley leaves infected with powdery mildew. New Phytol 1994, 126:213-222.
121. Bernfeld P. Amylases, α and β. Method Enzymol 1955, 1:149-158.