Different Structures in Humic Substances Lead to Impaired Germination but Increased Protection against Saline Stress in Corn

References

• Aguiar, N. O., L. O. Medici, F. L. Olivares, L. B. Dobbss, A. Torres-Netto, S. F. Silva, E. H. Novotny, and L. P. Canellas. 2016. Metabolic profile and antioxidant responses during drought stress recovery in sugarcane treated with humic acids and endophytic diazotrophic bacteria. Annals of Applied Biolology 168:203–13. doi:10.1111/aab.12256.
   Web of Science ®Google Scholar
• Aguiar, N. O., E. H. Novotny, A. L. Oliveira, V. M. Rumjanek, F. L. Olivares, and L. P. Canellas. 2013. Prediction of humic acids bioactivity using spectroscopy and multivariate analysis. Journal of Geochemical Explorer 129:95–102. doi:10.1016/j.gexplo.2012.10.005.
   Web of Science ®Google Scholar
• Aosa.1983. Association of official seed analysis. Seed Vigor Testing Handbook, pp. 93.
   Google Scholar
• Arnon, D. I. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vu lgaris. Plant Physiology 24:1–15. doi:10.1104/pp.24.1.1.
   PubMed Web of Science ®Google Scholar
• Asli, S., and P. M. Neumann. 2010. Rhizosphere humic acid interacts with root cell walls to reduce hydraulic conductivity and plant development. Plant and Soil 336:313–22. doi:10.1007/s11104-010-0483-2.
   Web of Science ®Google Scholar
• Barrs, H. D., and P. E. Weatherley. 1962. A re-examination of the relative turgidity technique for estimating water deficits in leaves. Australian Journal of Biological Science 15:413–28. doi:10.1071/BI9620413.
   Google Scholar
• Berbara, R. L., and A. C. García. 2014. Humic substances and plant defense metabolism. In Physiological mechanisms and adaptation strategies in plants under changing environment, ed. P. Ahmad, M. R. Wani, 297–319. New York: Springer. doi:10.1007/978-1-4614-8591-9-11.
   Google Scholar
• Brasil. 2009. Ministério da agricultura, pecuária e abastecimento. Regras para análise de sementes. Secretaria de Defesa Agropecuaria, in: Brasilia, DF: Mapa/ACS.395
   Google Scholar
• Canellas, L. P., and F. L. Olivares. 2014. Physiological responses to humic substances as plant growth promoter. Chemical and Biological Technologies in Agriculture 1:1–11. doi:10.1186/2196-5641-1-3.
   Google Scholar
• Canellas, L. P., F. L. Olivares., A. L. Okorokova-Façanha, and A. R. Façanha. 2002. Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots. Plant Physiology 130:1951–57. doi:10.1104/pp.007088.
   PubMed Web of Science ®Google Scholar
• Canellas, L. P., A. Piccolo, L. B. Dobbss., R. Spaccini, F. L. Olivares, D. B. Zandonadi, and A. R. Façanha. 2010. Chemical composition and bioactivity properties of size-fractions separated from a vermicompost humic acid. Chemosphere 78:457–66. doi:10.1016/j.chemosphere.2009.10.018.
   PubMed Web of Science ®Google Scholar
• Chen, Y., and T. Aviad. 1990. Effects of humic substances on plant growth. In Humic substances in soil and crop sciences: Selected readings, ed. P. MacCarthy, C. E. Clapp, R. L. Malcolm, and P. R. Bloom, 161–86. Madison, Wisconsin: American Society of Agronomy/Soil Science Society of America.
   Google Scholar
• Cordeiro, F. C., C. Santa-Catarina, V. Silveira, and S. R. de Souza. 2011. Humic acid effect on catalase activity and the generation of reactive oxygen species in corn (Zea mays). Bioscience, Biotechnology, and Biochemistry 75:70–74. doi:10.1271/bbb.100553.
   PubMed Web of Science ®Google Scholar
• Ferreira, D. F. 2014. Sisvar: a Guide for its Bootstrap procedures in multiple comparisons. Ciência e agrotecnologia 38:109–112. doi:10.1590/S1413-70542014000200001.
   Web of Science ®Google Scholar
• Dobbss, L. B., L. P. Canellas., F. L. Olivares., N. O. Aguiar, L. E. Peres, M. Azevedo, R. Spaccini, A. Piccolo, and A. R. Façanha. 2010. Bioactivity of chemically transformed humic matter from vermicompost on plant root growth. Journal of Agricultural and Food Chemistry 58:3681–88. doi:10.1021/jf904385c.
   PubMed Web of Science ®Google Scholar
• García, A. C., L. G. A. de Souza, M. G. Pereira, R. N. Castro, J. M. García-Mina, E. Zonta, F. J. G. Lisboa, and R. L. L. Berbara. 2016a. Structure-property-function relationship in humic substances to explain the biological activity in plants. Scientific Report 6:20798. doi:10.1038/srep20798.
   PubMed Web of Science ®Google Scholar
• García, A. C., P. Quintero, J. Javier, M. Balmori, H. López, and G. Izquierdo. 2016b. Effects of a humic liquid extract obtained from vermicompost on growing and yield corn. Revista Ciencias Técnicas Agropecuarias 25:38–43.
   Google Scholar
• García, A. C., L. A. Santos, L. G. A. de Souza, O. C. H. Tavares, E. Zonta, E. T. M. Gomes, J. M. García-Mina, and R. L. Berbara. 2016c. Vermicompost humic acids modulate the accumulation and metabolism of ROS in rice plants. Journal of Plant Physiology 192:56–63. doi:10.1016/j.jplph.2016.01.008.
   PubMed Web of Science ®Google Scholar
• García, A. C., L. A. Santos, F. G. Izquierdo, V. M. Rumjanek, R. N. Castro, F. S. Dos Santos, L. G. A. de Souza, and R. L. L. Berbara. 2014. Potentialities of vermicompost humic acids to alleviate water stress in rice plants (Oryza sativa L.). Journal of Geochemical Exploration 136:48–54. doi:10.1016/j.gexplo.2013.10.005.
   Web of Science ®Google Scholar
• García, A. C., L. A. Santos, F. G. Izquierdo, M. V. L. Sperandio, R. N. Castro, and R. L. L. Berbara. 2012. Vermicompost humic acids as an ecological pathway to protect rice plant against oxidative stress. Ecological Engineering 47:203–08. doi:10.1016/j.ecoleng.2012.06.011.
   Web of Science ®Google Scholar
• García-Mina, J. M., M. C. Antolín, and M. Sanchez-Diaz. 2004. Metal-humic complexes and plant micronutrient uptake: A study based on different plant species cultivated in diverse soil types. Plant and Soil 258:57–68. doi:10.1023/B:PLSO.0000016509.56780.40.
   Web of Science ®Google Scholar
• Hernández, V. G., O. H. González, I. F. Guridi, and F. N. Arbelo. 2012. Influência de la siembra directa y las aplicaciones foliares de extracto líquido de Vermicompost en el crecimiento y rendimiento del frijol. Revista Ciencias Tecnicas Agropecuarias 21:86–90.
   Google Scholar
• Labouriau, L. G., and M. E. B. Valadares. 1976. On the germination of seeds of Calotropis procera (Ait) Ait. f. Anais Da Academia Brasileira De Ciências (rio De Janeiro) 48:236–84.
   Web of Science ®Google Scholar
• Lichtenthaler, H. K. 1987. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148:350–82. doi:10.1016/0076-6879(87)48036-1.
   Web of Science ®Google Scholar
• Loffredo, E., A. J. Palazzo, N. Senesi, C. E. Clapp, and T. L. Bashore. 2010. Germination and early growth of slickspot peppergrass (Lepidium papilliferum) as affected by desert soil humic acids. Soil Science 175:186–93. doi:10.1097/SS.0b013e3181d9942e.
   Web of Science ®Google Scholar
• Lutts, S., J. M. Kinet., and J. Bouahrmont. 1996. NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Annals of Botany 78:389–98. doi:10.1006/anbo.1996.0134.
   Web of Science ®Google Scholar
• Maguire, J. D. 1962. Speed of germination-aid in selection and evaluation for seedling emergence and vigor 1. In Crop science2: 176–77.
   Google Scholar
• Monda, H., V. Cozzolino, G. Vinci, R. Spaccini, and A. Piccolo. 2017. Molecular characteristics of water-extractable organic matter from different composted biomasses and their effects on seed germination and early growth of maize. Science of Total Environment 590–591:40–49. doi:10.1016/j.scitotenv.2017.03.026.
   PubMed Web of Science ®Google Scholar
• Mora, V., R. Baigorri, E. Bacaicoa, A. M. Zamarreño, and J. M. García-Mina. 2012. The humic acid-induced changes in the root concentration of nitric oxide, IAA and ethylene do not explain the changes in root architecture caused by humic acid in cucumber. Environmental and Experimental Botany 76:24–32. doi:10.1016/j.envexpbot.2011.10.001.
   Web of Science ®Google Scholar
• Muscolo, A., M. Sidari, and S. Nardi. 2013. Humic substance: relationship between structure and activity. Deeper information suggests univocal findings. Journal of Geochemical Exploration 129:57–63. doi:10.1016/j.gexplo.2012.10.012.
   Web of Science ®Google Scholar
• Nakagawa, J. 1999. Testes de vigor baseados no desempenho das plântulas. In Vigor de sementes: conceitos e testes, ed. F. C. Krzyzanoswki, R. D. Vieira, and J. B. França Neto, 2.1–2.24, Editora Informativo Abrates, Londrina.
   Google Scholar
• Nebbioso, A., and A. Piccolo. 2012. Advances in humeomics: enhanced structural identification of humic molecules after size fractionation of a soil humic acid. Analytica Chimica Acta 720:77–90. doi:10.1016/j.aca.2012.01.027.
   PubMed Web of Science ®Google Scholar
• Nebbioso, A., A. Piccolo, M. Lamshöft, and M. Spiteller. 2014. Molecular characterization of an end-residue of humeomics applied to a soil humic acid. RSC Advances 4:23658–65. doi:10.1039/C4RA01619J.
   Web of Science ®Google Scholar
• Olaetxea, M., V. Mora, E. Bacaicoa, M. Garnica, M. Fuentes, E. Casanova, A. M. Zamarreño, J. C. Iriarte, D. Etayo, I. Ederra, et al. 2015. Abscisic acid regulation of root hydraulic conductivity and aquaporin gene expression is crucial to the plant shoot growth enhancement caused by rhizosphere humic acids. Plant Physiology 169:2587–96. doi:10.1104/pp.15.00596.
   PubMed Web of Science ®Google Scholar
• Piccolo, A. 1996. Humus and soil conservation. In Humic substances in terrestrial ecosystems, ed. A. Piccolo, 225–64. Amsterdam, Netherlands: Elsevier.
   Google Scholar
• Piccolo, A. 2001. The supramolecular structure of humic substances. Soil Science 166:810–32. doi:10.1097/00010694-200111000-00007.
   Web of Science ®Google Scholar
• R Development Core Team 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2011. http://www.r-project.org. accessed January 31, 2011
   Google Scholar
• Reis, G. G., and M. W. Muller. 1978. Análise de crescimento de plantas - mensuração do crescimento. Belém: CPATU.
   Google Scholar
• Rodrigues, L. A., C. Z. Alves, C. H. Q. Rego, T. R. B. D. Silva, and J. B. D. Silva. 2017. Humic acid on germination and vigor of corn seeds. Revista Caatinga 30:149–54. doi:10.1590/1983-21252017v30n116rc.
   Web of Science ®Google Scholar
• Schiavon, M., D. Pizzeghello, A. Muscolo, S. Vaccaro, O. Francioso, and S. Nardi. 2010. High molecular size humic substances enhance phenylpropanoid metabolism in maize (Zea mays L.). Journal of Chemical Ecology 36:662–69. doi:10.1007/s10886-010-9790-6.
   PubMed Web of Science ®Google Scholar
• Šerá, B., and F. Novák. 2011. The effect of humic substances on germination and early growth of Lamb’s Quarters (Chenopodium album agg.). Biologia 66/3:470. doi:10.2478/s11756-011-0037-y.
   Web of Science ®Google Scholar
• Song, G., E. H. Novotny, A. J. Simpson, C. E. Clapp, and M. H. B. Hayes. 2008. Sequential exhaustive extraction of a mollisol soil, and characterizations of humic components, including humin, by solid and solution state NMR. European Journal of Soil Science 59:505–16. doi:10.1111/j.1365-2389.2007.01006.x.
   Web of Science ®Google Scholar
• Stevenson, F. J. 1994. Humus chemistry: Genesis, composition, and reactions. 2nd ed. New York: Wiley-Interscience.
   Google Scholar
• Tan, K. H. 2014. Humic matter in soil and the environment: Principles and controversies. 2nd ed. Boca Raton, Florida: CRC Press.
   Google Scholar
• Trevisan, S., A. Botton, S. Vaccaro, A. Vezzaro, S. Quaggiotti, and S. Nardi. 2011. Humic substances affect Arabidopsis physiology by altering the expression of genes involved in primary metabolism, growth and development. Environmental and Experimental Botany 74:45–55. doi:10.1016/j.envexpbot.2011.04.017.
   Web of Science ®Google Scholar
• Trevisan, S., D. Pizzeghello, B. Ruperti, O. Francioso, A. Sassi, K. Palme, S. Quaggiotti, and S. Nardi. 2010. Humic substances induce lateral root formation and expression of the early auxin-responsive IAA19 gene and DR5 synthetic element in Arabidopsis. Plant Biology 12:604–14. doi:10.1111/j.1438-8677.2009.00248.x.
   PubMed Web of Science ®Google Scholar
• Varanini, Z., and R. Pinton. 2006. Plant-soil relationship: role of humic substances in iron nutrition. In Iron nutrition in plants and rhizospheric microorganisms, ed. L. L. Barton, J. Abadia, 153–68. Netherlands: Springer.
   Google Scholar
• WRB. 2015. International soil classification system for naming soils and creating legends for soil maps. In World reference base for soil resources 2014, 85–182.Rome: Food and Agriculture Organization of the United Nations.
   Google Scholar
• Zwiazek, J. J., and T. J. Blake. 1990. Effects of preconditioning on electrolyte leakage and lipid composition in black spruce (Picea mariana) stressed with polyethylene glycol. Plant Physiology 79:71–77. doi:10.1034/j.1399-3054.1990.790111.x.
   Google Scholar