Table of Contents Author Guidelines Submit a Manuscript
The Scientific World Journal
Volume 2015, Article ID 391234, 14 pages
http://dx.doi.org/10.1155/2015/391234
Research Article

Transcriptome Analysis of Gelatin Seed Treatment as a Biostimulant of Cucumber Plant Growth

Cornell University School of Integrated Plant Science, New York State Agriculture Experimental Station, Geneva, NY 24456, USA

Received 29 May 2015; Accepted 8 July 2015

Academic Editor: Zhoufei Wang

Copyright © 2015 H. T. Wilson et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. L. Takahashi and J. Trias, “Promotion of plant growth using collagen-based gelatin,” WO2012109522 A1, PCT/US2012/02417, 2012.
  2. E. Kunicki, A. Grabowska, A. Sekara, and R. Wojciechowska, “The effect of cultivar type, time of cultivation, and biostimulant treatment on the yield of spinach (Spinacia oleracea L.),” Folia Horticulturae, vol. 22, no. 2, 2010. View at Google Scholar
  3. R. Bulgari, G. Cocetta, A. Trivellini, P. Vernieri, and A. Ferrante, “Biostimulants and crop responses: a review,” Biological Agriculture and Horticulture, vol. 31, no. 1, pp. 1–17, 2015. View at Publisher · View at Google Scholar · View at Scopus
  4. V. Ziosi, R. Zandoli, A. Di Nardo, S. Biondi, F. Antognoni, and F. Calandriello, “Biological activity of different botanical extracts as evaluated by means of an array of in vitro and in vivo bioassays,” Acta Horticulturae, vol. 1009, pp. 61–66, 2012. View at Google Scholar · View at Scopus
  5. P. du Jardim, “The science of plant biostimulants—a bibliographic analysis. Contract 30-CE0455515/00-96, ad hoc study on bio-stimulants products,” 2012.
  6. European Biostimulants Industry Council, 2014, http://www.biostimulants.eu/.
  7. J. Parrado, J. Bautista, E. J. Romero, A. M. García-Martínez, V. Friaza, and M. Tejada, “Production of a carob enzymatic extract: potential use as a biofertilizer,” Bioresource Technology, vol. 99, no. 7, pp. 2312–2318, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Koukounaras, P. Tsouvaltzis, and A. S. Siomos, “Effect of root and foliar application of amino acids on the growth and yield of greenhouse tomato in different fertilization levels,” Journal of Food, Agriculture and Environment, vol. 11, no. 2, pp. 644–648, 2013. View at Google Scholar · View at Scopus
  9. J. P. Morales-Payan and W. M. Stall, “Papaya (Carica papaya) response to foliar treatments with organic complexes of peptides and amino acids,” Proceedings of the Florida State Horticultural Society, vol. 116, pp. 30–31, 2003. View at Google Scholar
  10. A. Ertani, M. Schiavon, A. Muscolo, and S. Nardi, “Alfalfa plant-derived biostimulant stimulate short-term growth of salt stressed Zea mays L. plants,” Plant and Soil, vol. 364, no. 1-2, pp. 145–158, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Ertani, D. Pizzeghello, A. Altissimo, and S. Nardi, “Use of meat hydrolyzate derived from tanning residues as plant biostimulant for hydroponically grown maize,” Journal of Plant Nutrition and Soil Science, vol. 176, no. 2, pp. 287–295, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Grabowska, E. Kunicki, A. Sękara, A. Kalisz, and R. Wojciechowska, “The effect of cultivar and biostimulant treatment on the carrot yield and its quality,” Vegetable Crops Research Bulletin, vol. 77, no. 1, pp. 37–48, 2012. View at Google Scholar
  13. G. Colla, E. Svecova, Y. Rouphael et al., “Effectiveness of a plant-derived protein Hydrolysate to improve crop performances under different growing conditions,” Acta Horticulturae, vol. 1009, pp. 175–180, 2012. View at Google Scholar · View at Scopus
  14. L. Lucini, Y. Rouphael, M. Cardarelli, R. Canaguier, P. Kumar, and G. Colla, “The effect of a plant-derived biostimulant on metabolic profiling and crop performance of lettuce grown under saline conditions,” Scientia Horticulturae, vol. 182, pp. 124–133, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Boehme, Y. Schevschenko, and I. Pinker, “Use of biostimulators to reduce abiotics stress in cucumber plants (Cucumis sativus L.),” Acta Horticulturae, vol. 774, pp. 339–344, 2008. View at Google Scholar · View at Scopus
  16. M. Boehme, J. Schevtschenko, and I. Pinker, “Plant nutrition—effect of biostimulators on growth of vegetables in hydroponical systems,” Acta Horticulturae, vol. 697, pp. 337–344, 2005. View at Google Scholar · View at Scopus
  17. A. Przybysz, H. Gawrońska, and J. Gajc-Wolska, “Biological mode of action of a nitrophenolates-based biostimulant: case study,” Frontiers in Plant Science, vol. 5, article 713, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Parađiković, T. Vinković, I. Vinković Vrček, I. Žuntar, M. Bojic, and M. Medić-Šarić, “Effect of natural biostimulants on yield and nutritional quality: an example of sweet yellow pepper (Capsicum annuum L.) plants,” Journal of the Science of Food and Agriculture, vol. 91, no. 12, pp. 2146–2152, 2011. View at Publisher · View at Google Scholar
  19. A. Petrozza, A. Santaniello, S. Summerer et al., “Physiological responses to Megafol treatments in tomato plants under drought stress: a phenomic and molecular approach,” Scientia Horticulturae, vol. 174, no. 1, pp. 185–192, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. G. L. Kauffman III, D. P. Kneivel, and T. L. Watschke, “Effects of a biostimulant on the heat tolerance associated with photosynthetic capacity, membrane thermostability, and polyphenol production of perennial ryegrass,” Crop Science, vol. 47, no. 1, pp. 261–267, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. K. C. Jisha and J. T. Puthur, “Seed priming with BABA (β-amino butyric acid): a cost-effective method of abiotic stress tolerance in Vigna radiata (L.) Wilczek,” Protoplasma, 2015. View at Publisher · View at Google Scholar
  22. M. Schiavon, A. Ertani, and S. Nardi, “Effects of an alfalfa protein hydrolysate on the gene expression and activity of enzymes of the tricarboxylic acid (TCA) cycle and nitrogen metabolism in Zea mays L,” Journal of Agricultural and Food Chemistry, vol. 56, no. 24, pp. 11800–11808, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Ertani, L. Cavani, D. Pizzeghello et al., “Biostimulant activity of two protein hydrolyzates in the growth and nitrogen metabolism of maize seedlings,” Journal of Plant Nutrition and Soil Science, vol. 172, no. 2, pp. 237–244, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Maini, “The experience of the first biostimulant, based on amino acids and peptides: a short retrospective review on the laboratory researches and practival results,” Fertilitas Agrorum, vol. 1, pp. 29–43, 2006. View at Google Scholar
  25. P. Calvo, L. Nelson, and J. W. Kloepper, “Agricultural uses of plant biostimulants,” Plant and Soil, vol. 383, pp. 3–41, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Vaccaro, A. Ertani, A. Nebbioso et al., “Humic substances stimulate maize nitrogen assimilation and amino acid metabolism at physiological and molecular level,” Chemical and Biological Technologies in Agriculture, vol. 2, no. 1, pp. 1–12, 2015. View at Publisher · View at Google Scholar
  27. Z. Li, Z. Zhang, P. Yan, S. Huang, Z. Fei, and K. Lin, “RNA-Seq improves annotation of protein-coding genes in the cucumber genome,” BMC Genomics, vol. 12, article 540, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. K. A. Baggerly, L. Deng, J. S. Morris, and C. M. Aldaz, “Differential expression in SAGE: accounting for normal between-library variation,” Bioinformatics, vol. 19, no. 12, pp. 1477–1483, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Langfelder and S. Horvath, “WGCNA: an R package for weighted correlation network analysis,” BMC Bioinformatics, vol. 9, article 559, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. C. A. Hollender, C. Kang, O. Darwish et al., “Floral transcriptomes in woodland strawberry uncover developing receptacle and anther gene networks,” Plant Physiology, vol. 165, no. 3, pp. 1062–1075, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. F. M. You, N. Huo, Y. Q. Gu et al., “BatchPrimer3: a high throughput web application for PCR and sequencing primer design,” BMC Bioinformatics, vol. 9, article 253, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. D. Fraga, T. Meulia, and S. Fenster, “Real-time PCR,” Current Protocols—Essential Laboratory Techniques, vol. 10, pp. 10.3.1–10.3.33, 2008. View at Google Scholar
  33. M. W. Pfaffl, “A new mathematical model for relative quantification in real-time RT-PCR,” Nucleic Acids Research, vol. 29, no. 9, article e45, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Assenov, F. Ramírez, S. E. Schelhorn, T. Lengauer, and M. Albrecht, “Computing topological parameters of biological networks,” Bioinformatics, vol. 24, no. 2, pp. 282–284, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. G. Balian and J. H. Bowes, “The structure and properties of collagen,” in The Science and Technology of Gelatin, A. G. Ward and A. Courts, Eds., pp. 1–27, Academic Press, London, UK, 1977. View at Google Scholar
  36. R. Schrieber and H. Gareis, Gelatin Handbook: Theory and Industrial Practice, Wiley, 2007.
  37. J. M. Regenstein and G. Boran, “Fish gelatin,” Advances in Food and Nutrition Research, vol. 60, pp. 119–143, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Näsholm, K. Kielland, and U. Ganeteg, “Uptake of organic nitrogen by plants,” New Phytologist, vol. 182, no. 1, pp. 31–48, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Schmidt and G. R. Stewart, “Glycine metabolism by plant roots and its occurrence in Australian plant communities,” Australian Journal of Plant Physiology, vol. 26, no. 3, pp. 253–264, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. B. Thornton, S. M. Osborne, E. Paterson, and P. Cash, “A proteomic and targeted metabolomic approach to investigate change in Lolium perenne roots when challenged with glycine,” Journal of Experimental Botany, vol. 58, no. 7, pp. 1581–1590, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. H.-J. Wang, L.-H. Wu, M.-Y. Wang, Y.-H. Zhu, Q.-N. Tao, and F.-S. Zhang, “Effects of amino acids replacing nitrate on growth, nitrate accumulation, and macroelement concentrations in Pak-choi (Brassica chinensis L .),” Pedosphere, vol. 17, no. 5, pp. 595–600, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. X.-L. Wang, W.-J. Yu, Q. Zhou, R.-F. Han, and D.-F. Huang, “Metabolic response of Pakchoi leaves to amino acid nitrogen,” Journal of Integrative Agriculture, vol. 13, no. 4, pp. 778–788, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Ortiz-Lopez, H.-C. Chang, and D. R. Bush, “Amino acid transporters in plants,” Biochimica et Biophysica Acta, vol. 1465, no. 1-2, pp. 275–280, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. X. Liu and D. R. Bush, “Expression and transcriptional regulation of amino acid transporters in plants,” Amino Acids, vol. 30, no. 2, pp. 113–120, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. M. G. Guo, Molecular and Genomic Analysis of Nitrogen Regulation of Amino Acid Permease I (AAP1) in Arabidopsis, University of Illinois at Urbana-Champaign, 2004.
  46. W. N. Fischer, B. André, D. Rentsch et al., “Amino acid transport in plants,” Trends in Plant Science, vol. 3, no. 5, pp. 188–195, 1998. View at Publisher · View at Google Scholar · View at Scopus
  47. C. Schobert, W. Köckenberger, and E. Komor, “Uptake of amino acids by plants from the soil: a comparative study with castor bean seedlings grown under natural and axenic soil conditions,” Plant and Soil, vol. 109, no. 2, pp. 181–188, 1988. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Okumoto, R. Schmidt, M. Tegeder et al., “High affinity amino acid transporters specifically expressed in xylem parenchyma and developing seeds of Arabidopsis,” The Journal of Biological Chemistry, vol. 277, no. 47, pp. 45338–45346, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Okumoto, W. Koch, M. Tegeder et al., “Root phloem-specific expression of the plasma membrane amino acid proton co-transporter AAP3,” Journal of Experimental Botany, vol. 55, no. 406, pp. 2155–2168, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. H. H. Marella, E. Nielsen, D. P. Schachtman, and C. G. Taylor, “The amino acid permeases AAP3 and AAP6 are involved in root-knot nematode parasitism of Arabidopsis,” Molecular Plant-Microbe Interactions, vol. 26, no. 1, pp. 44–54, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. W.-N. Fischer, D. D. F. Loo, W. Koch et al., “Low and high affinity amino acid H+-cotransporters for cellular import of neutral and charged amino acids,” Plant Journal, vol. 29, no. 6, pp. 717–731, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. D. Rentsch, B. Hirner, E. Schmelzer, and W. B. Frommer, “Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant,” Plant Cell, vol. 8, no. 8, pp. 1437–1446, 1996. View at Publisher · View at Google Scholar · View at Scopus
  53. E. Hunt, S. Gattolin, H. J. Newbury et al., “A mutation in amino acid permease AAP6 reduces the amino acid content of the Arabidopsis sieve elements but leaves aphid herbivores unaffected,” Journal of Experimental Botany, vol. 61, no. 1, pp. 55–64, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Niittylä, A. T. Fuglsang, M. G. Palmgren, W. B. Frommer, and W. X. Schulze, “Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis,” Molecular & Cellular Proteomics, vol. 6, no. 10, pp. 1711–1726, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. V. Vitart, I. Baxter, P. Doerner, and J. F. Harper, “Evidence for a role in growth and salt resistance of a plasma membrane H+-ATPase in the root endodermis,” Plant Journal, vol. 27, no. 3, pp. 191–201, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. N. D. Dewitt, B. Hong, M. R. Sussman, and J. F. Harper, “Targeting of two Arabidopsis H+-ATPase isoforms to the plasma membrane,” Plant Physiology, vol. 112, no. 2, pp. 833–844, 1996. View at Publisher · View at Google Scholar · View at Scopus
  57. J. F. Harper, L. Manney, and M. R. Sussman, “The plasma membrane H+-ATPase gene family in Arabidopsis: genomic sequence of AHA10 which is expressed primarily in developing seeds,” Molecular & General Genetics, vol. 244, no. 6, pp. 572–587, 1994. View at Publisher · View at Google Scholar · View at Scopus
  58. K. J. Boorer, W. B. Frommer, D. R. Bush, M. Kreman, D. D. F. Loo, and E. M. Wright, “Kinetics and specificity of a H+/amino acid transporter from Arabidopsis thaliana,” The Journal of Biological Chemistry, vol. 271, no. 4, pp. 2213–2220, 1996. View at Publisher · View at Google Scholar · View at Scopus
  59. K. J. Boorer and W. N. Fischer, “Specificity and stoichiometry of the Arabidopsis H+/amino acid transporter AAP5,” The Journal of Biological Chemistry, vol. 272, no. 20, pp. 13040–13046, 1997. View at Publisher · View at Google Scholar
  60. D. Loqué and N. von Wirén, “Regulatory levels for the transport of ammonium in plant roots,” Journal of Experimental Botany, vol. 55, no. 401, pp. 1293–1305, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. B. Neuhäuser, M. Dynowski, and U. Ludewig, “Channel-like NH3 flux by ammonium transporter AtAMT2,” FEBS Letters, vol. 583, no. 17, pp. 2833–2838, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. C. Sohlenkamp, C. C. Wood, G. W. Roeb, and M. K. Udvardi, “Characterization of Arabidopsis AtAMT2, a high-affinity ammonium transporter of the plasma membrane,” Plant Physiology, vol. 130, no. 4, pp. 1788–1796, 2002. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Khademi, J. I. O'Connell, J. Remis, Y. Robles-Colmenares, L. J. W. Miercke, and R. M. Stroud, “Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 Å,” Science, vol. 305, no. 5690, pp. 1587–1594, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. H. Kato, T. Motomura, Y. Komeda, T. Saito, and A. Kato, “Overexpression of the NAC transcription factor family gene ANAC036 results in a dwarf phenotype in Arabidopsis thaliana,” Journal of Plant Physiology, vol. 167, no. 7, pp. 571–577, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. A. N. Olsen, H. A. Ernst, L. L. Leggio, and K. Skriver, “NAC transcription factors: structurally distinct, functionally diverse,” Trends in Plant Science, vol. 10, no. 2, pp. 79–87, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Aida, T. Ishida, H. Fukaki, H. Fujisawa, and M. Tasaka, “Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant,” Plant Cell, vol. 9, no. 6, pp. 841–857, 1997. View at Publisher · View at Google Scholar · View at Scopus
  67. K. Kikuchi, M. Ueguchi-Tanaka, K. T. Yoshida, Y. Nagato, M. Matsusoka, and H.-Y. Hirano, “Molecular analysis of the NAC gene family in rice,” Molecular and General Genetics, vol. 262, no. 6, pp. 1047–1051, 2000. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Duval, T.-F. Hsieh, S. Y. Kim, and T. L. Thomas, “Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily,” Plant Molecular Biology, vol. 50, no. 2, pp. 237–248, 2002. View at Publisher · View at Google Scholar · View at Scopus
  69. H. Ooka, K. Satoh, K. Doi et al., “Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana,” DNA Research, vol. 10, no. 6, pp. 239–247, 2003. View at Publisher · View at Google Scholar · View at Scopus
  70. J. O. D. Coleman, M. M. A. Blake-Kalff, and T. G. E. Davies, “Detoxification of xenobiotics by plants: chemical modification and vacuolar compartmentation,” Trends in Plant Science, vol. 2, no. 4, pp. 144–151, 1997. View at Publisher · View at Google Scholar · View at Scopus
  71. M. C. J. Wilce and M. W. Parker, “Structure and function of glutathione S-transferases,” Biochimica et Biophysica Acta—Protein Structure and Molecular Enzymology, vol. 1205, no. 1, pp. 1–18, 1994. View at Publisher · View at Google Scholar · View at Scopus
  72. D. P. Dixon and R. Edwards, “Glutathione transferases,” The Arabidopsis Book, vol. 8, no. 8, Article ID e0131, 2010. View at Google Scholar
  73. D. P. Dixon, A. Lapthorn, and R. Edwards, “Plant glutathione transferases,” Genome Biology, vol. 3, 2002. View at Google Scholar
  74. L. F. Thatcher, C. Carrie, C. R. Andersson, K. Sivasithamparam, J. Whelan, and K. B. Singh, “Differential gene expression and subcellular targeting of Arabidopsis glutathione S-transferase F8 is achieved through alternative transcription start sites,” Journal of Biological Chemistry, vol. 282, no. 39, pp. 28915–28928, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. E. Martinoia, M. Klein, M. Geisler et al., “Multifunctionality of plant ABC transporters—more than just detoxifiers,” Planta, vol. 214, no. 3, pp. 345–355, 2002. View at Publisher · View at Google Scholar · View at Scopus