Change in ATP-binding cassette B1/19, glutamine synthetase and alcohol dehydrogenase gene expression during root elongation in Betula pendula Roth and Alnus glutinosa L. Gaertn in response to leachate and leonardite humic substances
[en] Humic substances (HS) are complex and heterogeneous compounds of humified organic matter resulting from the chemical and microbiological decomposition of organic residues. HS have a positive effect on plant growth and development by improving soil structure and fertility. They have long been recognized as plant growth-promoting substances, particularly with regard to influencing nutrient uptake, root growth and architecture. The biochemical and molecular mechanisms through which HS influence plant physiology are not well understood. This study evaluated the bioactivity of landfill leachate and leonardite HS on alder (Alnus glutinosa L. Gaertn) and birch (Betula pendula Roth) during root elongation in vitro. Changes in root development were studied in relation to auxin, carbon and nitrogen metabolisms, as well as to the stress adaptive response. The cDNA fragments of putative genes encoding two ATP-binding cassette (ABC) transporters (ABCB1 and ABCB19) belonging to the B subfamily of plant ABC auxin transporters were cloned and sequenced. Molecular data indicate that HS and their humic acid (HA) fractions induce root growth by influencing polar auxin transport (PAT), as illustrated by the modulation of the ABCB transporter transcript levels (ABCB1 and ABCB19). There were also changes in alcohol dehydrogenase (ADH) and glutamine synthetase (GS) gene transcript levels in response to HS exposure. These findings confirmed that humic matter affects plant growth and development through various metabolic pathways, including hormonal, carbon and nitrogen metabolisms and stress response or signalization.
Change in ATP-binding cassette B1/19, glutamine synthetase and alcohol dehydrogenase gene expression during root elongation in Betula pendula Roth and Alnus glutinosa L. Gaertn in response to leachate and leonardite humic substances
Adani F., Genevini P., Tambone F., Montoneri E. Compost effect on soil humic acid: a NMR study. Chemosphere 2006, 65:1414-1418. 10.1016/j.chemosphere.2006.03.070.
Aguirre E., Leménager D., Bacaicoa E., Fuentes M., Baigorri R., Zamarreño A.M., García-Mina J.M. The root application of a purified leonardite humic acid modifies the transcriptional regulation of the main physiological root responses to Fe deficiency in Fe-sufficient cucumber plants. Plant Physiol. Biochem. 2009, 47:215-223. 10.1016/j.plaphy.2008.11.013.
Aiken G.R., McKnight G.R., Wershaw R.L., MacCarthy P. Humic Substances in Soil, Sediment and Water - Geochemistry, Isolation and Characterization 1985, Wiley, New York. 10.1002/gj.3350210213.
Bagh K., Hiraoki T., Thorpe T.A., Vogel H.J. Nitrogen-15 NMR studies of nitrogen metabolism in Picea glauca buds. Plant Physiol. Biochem. 2004, 42:803-809. 10.1016/j.plaphy.2004.09.006.
Bajji M., Druart P. Protocol development for in vitro assessment of cadmium tolerance in black alder and basket willow at the callus and whole plant levels. Acta Hort. 2012, 961:123-131.
Berbara R.L.L., García A.C. Humic substances and plant defense metabolism. Physiological Mechanisms and Adaptation Strategies in Plants under Changing Environment 2014, vol. 1:297-319. Springer, New York. 10.1007/978-1-4614-8591-9_11.
Billard V., Etienne Ph., Jannin L., Garnica M., Cruz F., Garcia-Mina J.M., Yvin J.C., Ourry A. Two biostimulants derived from algae or humic acid induce similar responses in the mineral content and gene expression of winter oilseed rape (Brassica napus L.). J. Plant. Growth Regul. 2014, 33:305-316. 10.1007/s00344-013-9372-2.
Canellas L.P., Olivares F.L. Physiological responses to humic substances as plant growth promoter. Chem. Boil. Technol. Agric. 2014, 1(3):1-12. 10.1186/2196-5641-1-3.
Canellas L.P., Spaccini R., Piccolo A., Dobbss L.B., Okorokova-Façanha A.L., Santos G.A., Olivares F.L., Façanha A.R. Relationships between chemical characteristics and root growth promotion of humic acids isolated from Brazilian oxisols. Soil Sci. 2009, 174:611-620. 10.1097/SS.0b013e3181bf1e03.
Chen Y., Avaid T. Effects of humic substances on plant growth. Humic Substances in Soil and Crop Sciences: selected Readings 1990, 161-186. American Society of agronomy and Soil Science Society of America, Madison. P. MaCcarthy, C.E. Capp, R.L. Malcolm, P.R. Bloom (Eds.).
Cho M., Cho H.T. The function of ABCB transporters in auxin transport. Plant Signal. Behav. 2013, 8(2):e22990. 10.1104/pp.112.196139.
Chung H.J., Ferl R.J. Arabidopsis alcohol dehydrogenase expression in both shoots and roots is conditioned by root growth environment. Plant Physiol. 1999, 121:429-436. 10.1104/pp.121.2.429.
Cordeiro F.C., Santa-Catarina C., Silveira V., de Souza S.R. Humic acid effect on catalase activity and the generation of reactive oxygen species in corn (Zea Mays L). Biosci. Biotechnol. Biochem. 2011, 75:70-74. 10.1271/bbb.100553.
Druart Ph. Micropropagation of Prunus species relevant to cherry fruit production. Methods Mol. Biol. 2013, 994:119-136. 10.1007/978-1-62703-074-8_9. M. Lambardi, E.A. Ozudogru, S.M. Jain (Eds.).
Druart Ph Optimization of culture media for in vitro rooting of Malus domestica Borkh. cv. Compact Spartan. Biol. Plant. 1997, 39:67-77. 10.1023/A:1000309023415.
Ertani A., Francioso O., Tugnoli V., Righi V., Nardi S. Effect of commercial lignosulfonate-humate on Zea mays L. metabolism. J. Agric. Food. Chem. 2011, 59:11940-11948. 10.1021/jf202473e.
Ertani A., Pizzeghello D., Baglieri A., Cadili V., Tambone F., Gennari M., Nardi S. Humic-like substances from agro-industrial residues affect growth and nitrogen assimilation in maize (Zea mays L.) plantlets. J. Geochem. Explor. 2013, 129:103-111. 10.1016/j.gexplo.2012.10.001.
Fan T.W.M. Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog. Nucl. Magn. Reson. Spectrosc. 1996, 28:161-219. 10.1016/0079-6565(95)01017-3.
Gambino G., Perrone I., Gribaudo I. A rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochem. Anal. 2008, 19(6):520-525. 10.1002/pca.1078.
García A.C., Santos L.A., Izquierdo F.G., Sperandio M.V.L., Castro R.N., Berbara R.L.L. Vermicompost humic acids as an ecological pathway to protect rice plant against oxidative stress. Ecol. Eng. 2012, 47:203-208. 10.1016/j.ecoleng.2012.06.011.
Geisler M. Plant ABC Transporters. Signaling and Communication in Plants 2014, Springer, 333 pp.
Geldner N., Friml J., Stierhof Y.D., Jürgens G., Palme K. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 2001, 413:425-428. 10.1038/35096571.
Ingram P.A., Malamy J.E. Root system architecture. Advances in Botanical Research 2010, 75-117. Academic Press/Elsevier, New York. J.C. Kader, M. Delseny (Eds.).
Jannin L., Arkoun M., Ourry A., Laîné Ph., Goux D., Garnica M., Fuentes M., San Francisco S., Baigorri R., Cruz F., Houdusse F., Garcia-Mina J.M., Yvin J.C., Etienne Ph Microarray analysis of humic acid effects on Brassica napus growth: Involvement of N, C and S metabolisms. Plant Soil 2012, 359:297-319. 10.1007/s11104-012-1191-x.
Järvinen P., Palmé A., Morales L.O., Lännenpää M., Keinänen M., Sopanen T., Lascoux M. Phylogenetic relationships of Betula species (Betulaceae) based on nuclear ADH and chloroplast matK sequences. Am. J. Bot. 2004, 91(11):1834-1845. 10.3732/ajb.91.11.1834.
Kang J., Park J., Choi H., Burla B., Kretzschmar T., Lee Y., Martinoia E. Plant ABC transporters. Arabidopsis Book 2011, 9:2-25. 10.1199/tab.0153.
Kang K.H., Shin H.S., Park H. Characterization of humic substances present in landfill leachates with different ages and implications. Water Res. 2002, 36(16):4023-4032. 10.1016/S0043-1354(02)00114-8.
Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2δδCT Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262.
Malamy J.E. Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ. 2005, 28(1):67-77. 10.1111/j.1365-3040.2005.01306.x.
Mora V., Bacaicoa E., Zamarren A.M., Aguirre E., Garnica M., Fuentes M., Garcia-Mina J.M. Action of humic acid on promotion of cucumber shoot growth involves nitrate-related changes associated with the root-to-shoot distribution of cytokinins, polyamines and mineral nutrients. J. Plant Physiol. 2010, 167:633-642. 10.1016/j.jplph.2009.11.018.
Muscolo A., Cutrupi S., Nardi S. IAA detection in humic substances. Soil Biol. Biochem. 1998, 30:1199-1201. 10.1016/S0038-0717(98)00005-4.
Muscolo A., Sidari M., Attinà E., Francioso O., Tugnoli V., Nardi S. Biological activity of humic substances is related to their chemical structure. Soil Sci. Soc. Am. J. 2007, 71:75-85. 10.2136/sssaj2006.0055.
Muscolo A., Sidari M., Francioso O., Tugnoli V., Nardi S. The auxin-like activity of humic substances is related to membrane interactions in carrot cell culture. J. Chem. Ecol. 2007, 33:115-129. 10.1007/s10886-006-9206-9.
Muscolo A., Sidari M., Nardi S. Humic substance: relationship between structure and activity. Deeper information suggests univocal findings. J. Geochem. Explor. 2013, 129:57-63. 10.1016/j.gexplo.2012.10.012.
Nardi S., Carletti P., Pizzeghello D., Muscolo A. Biological activities of humic substances. Biophysico-chemical Processes Involving Natural Nonliving Organic Matter in Environmental Systems 2009, 305-339. John Wiley & Sons, Hoboken, New Jersey. N. Senesi, B. Xing, P.M. Huang (Eds.).
Nardi S., Panuccio M.R., Abenavoli M.R., Muscolo A. Auxin-like effect of humic substances extracted from faeces of Allolobophora caliginosa and A. rosea. Soil Biol. Biochem. 1994, 26:1341-1346. 10.1016/0038-0717(94)90215-1.
O'Donnell R.W. The auxin-like effects of humic preparations from leonardite. Soil Sci. 1973, 116(2):106-112.
Overvoorde P., Fukaki H., Beeckman T. Auxin control of root development. Cold Spring Harb. Perspect. Biol. 2010, 2:a001537. 10.1101/cshperspect.a001537.
Santelia D., Vincenzetti V., Azzarello E., Bovet L., Fukao Y., Düchtig P., Mancuso S., Martinoia E., Geisler M. MDR-like ABC transporter AtPGP4 involved in auxin-mediated lateral root and root hair development. FEBS Lett. 2005, 579:5399-5406. 10.1016/j.febslet.2005.08.061.
Siani S., Sharma I., Kaur N., Pati P.K. Auxin: a master regulator in plant root development. Plant Cell Rep. 2013, 32:741-757. 10.1007/s00299-013-1430-5.
Sidler M., Hassa P., Hasan S., Ringli C., Dudler R. Involvement of an ABC transporter in a developmental pathway regulating hypocotyl cell elongation in the light. Plant Cell 1998, 10:1623-1636. 10.1105/tpc.10.10.1623.
Sorin C., Bussell J.D., Camus I., Ljung K., Kowalczyk M., Geiss G. Auxin and light control of adventitious rooting in Arabidopsis require ARGONAUTE1. Plant Cell 2005, 17(5):1343-1359. 10.1105/tpc.105.031625.
Stevenson F.J. Humus Chemistry. Genesis, Composition, Reactions 1994, John Wiley & Sons, New York, 496 pp. second ed.
Sukumar P., Maloney G.S., Muday G.K. Localized induction of the ATP-binding cassette B19 auxin transporter enhances adventitious root formation in Arabidopsis. Plant Physiol. 2013, 162:1392-1405. 10.1104/pp.113.217174.
Tahiri A., Destain J., Druart Ph., Thonart Ph. Propriétés physico-chimiques et biologiques des substances humiques en relation avec le développement végétal. Biotechnol. Agron. Soc. Environ. 2014, 18(3):336-345.
Tahiri A., Destain J., Thonart Ph., Druart Ph In vitro model to study the biological properties of humic fractions from landfill leachate and leonardite during root elongation of Alnus glutinosa L. Gaertn and Betula pendula Roth. Plant Cell Tissue Organ Cult. 2015, 122(3):739-749. 10.1007/s11240-015-0807-2.
Tahiri, A., Richel A., Destain, J., Druart, Ph., Thonart, Ph., Ongena M. Comprehensive comparison of chemical and structural characterization of landfill leachate and leonardite humic fractions (submitted for publication).
Trevisan S., Pizzeghello D., Ruperti B., Francioso O., Sassi A., Palme K., Quaggiotti S., Nardi S. Humic substances induce lateral root formation and expression of the early auxin-responsive IAA19 gene and DR5 synthetic element in Arabidopsis. Plant Biol. 2010, 12:604-614. 10.1111/j.1438-8677.2009.00248.x.
Trevisan S., Francioso O., Quaggiotti S., Nardi S. Humic substances biological activity at the plant-soil interface: from environmental aspects to molecular factors. Plant Signal. Behav. 2010, 5(6):635-643.
Trevisan S., Botton A., Vaccaro S., Vezzaro A., Quaggiotti S., Nardi S. Humic substances affect Arabidopsis physiology by altering the expression of genes involved in primary metabolism, growth and development. Environ. Exp. Bot. 2011, 74:45-55. 10.1016/j.envexpbot.2011.04.017.
Tsuda E., Yang H., Nishimura T., Uehara Y., Sakai T., Furutani M., Koshiba T., Hirose M., Nozaki H., Murphy A.S., Hayashi K. Alkoxy-auxins are selective inhibitors of auxin transport mediated by PIN, ABCB, and AUX1 transporters. J. Biol. Chem. 2011, 286:2354-2364. 10.1074/jbc.M110.171165.
Vaccaro S., Ertani A., Nebbioso A., Muscolo A., Quaggiotti S., Piccolo A., Nardi S. Humic substances stimulate maize nitrogen assimilation and amino acid metabolism at physiological and molecular level. Chem. Boil. Technol. Agric. 2015, 2(5):1-12. 10.1186/s40538-015-0033-5.
Walter A., Silk W.K., Schurr U. Environmental effects on spatial and temporal patterns of leaf and root growth. Annu. Rev. Plant Biol. 2009, 60:279-304. 10.1146/annurev.arplant.59.032607.092819.
Wickert E., Marcondes J., Lemos M.V., Lemos E.G.M. Nitrogen assimilation in Citrus based on CitEST data mining. Genet. Mol. Biol. 2007, 30(3S):810-818. 10.1590/S1415-47572007000500009.
Zandonadi D.B., Canellas L.P., Facxanha A.R. Indol-acetic and humic acids induce lateral root development through a concerted plasmalemma and tonoplast H+ pumps activation. Planta 2007, 225:1583-1595. 10.1007/s00425-006-0454-2.