Plant physiology as affected by humified organic matter

Zandonadi, Daniel Basílio; Santos, Mirella Pupo; Busato, Jader Galba; Peres, Lázaro Eustáquio Pereira; Façanha, Arnoldo Rocha

Abstract

Since the beginning of Human civilization, the soil organic matter has been used as plant growth promoter and/or regulator. Indeed, early in plant science history, even before the auxin concept has been established, the term "auximones" was coined to describe plant growth promoting humic acids derived from peat. Despite of this, until the end of the 20th century, humic substances remained as some of the most neglected environment signals in plant physiology research. However, this scenario has changed in last decade with the discovery that the major systems of energy transduction of the plant cell membranes, the proton pumps, can be tightly orchestrated by humic substances just as elicited by a hormonal signaling. Differential activations of both plasma membrane (PM H+-ATPase) and vacuolar pumps (V-ATPase and H+-PPase) are modulated by humic substances triggering ion signatures related to specific patterns of plant growth and development. Phytohormones have been found to be associated with this humus bioactivity, and nitric oxide acting as a second messenger in a signaling pathway in which plants can sense the soil environment to cope with specific conditions. In this review, we discuss some of the most influential data available in literature, which have shaped this underexplored interface between the chemistry of the organic matter and the plant physiology. The key role of organic matter in the sustainable agriculture will also be highlighted from a biochemical perspective of the plant cell responses to biofertilization, specially in tropical environments.

auxin; biofertilizer; humus; proton pumps; vegetables; vermicompost

Albuzio A, Ferrari G (1989) Modulation of the molecular size of humic substances by organic acids of the root exudates. Plant Soil 113:237-241.
Arancon NQ, Pant A, Radovich T, Hue NV, Potter JK, Converse CE (2012) Seed germination and seedling growth of tomato and lettuce as affected by vermicompost water extracts (Teas). HortScience 47:1722-1728.
Arteaga M, Garcés N, Novo R, Guridi F, Pino JA, Acosta M, Pasos M, Besú D (2007) Influencia de la aplicación foliar del bioestimulante Liplant sobre algunos indicadores biológicos del suelo. Revista de Protección Vegetal 22:110-117.
Bottomley WB (1914) Some accessory factors in plant growth and nutrition. Proceedings of the Royal Society of London-B 88:237-247.
Bottomley WB (1915) A bacterial test for plant food accessories: (auximones). Proceedings of the Royal Society of London-B 89:102-108
Bottomley WB (1917) Some effects of organic growth-promoting substances: (auximones) on the growth of Lemna minor in mineral culture solutions. Proceedings of the Royal Society of London-B 89:481-507.
Busato JG, Lima L, Aguiar NO, Canellas LP, Olivares FL (2012) Changes in labile phosphorus forms during maturation of vermicompost enriched with phosphorus-solubilizing and diazotrophic bacteria. Bioresource Technology 110:390-395.
Cacco G, Dell'Agnola G (1984) Plant growth regulator activity of soluble humic complex. Canadian Journal of Soil Science 62:306-310.
Cameron RS, Thornton BK, Swift RS, Posner AM (1972) Molecular weight and shape of humic acid from sedimentation and diffusion measurements on fractionated extracts. Journal of Soil Science 23:394-408.
Campos-Cuevas JC, Pelagio-Flores R, Raya-González J, Méndez-Bravo A, Ortiz-Castro R, López-Bucio J (2008) Tissue culture of Arabidopsis thaliana explants reveals a stimulatory effect of alkamides on adventitious root formation and nitric oxide accumulation. Plant Science 174:165-173.
Canellas LP, Olivares FL, Okorokova-Façanha AL, Façanha AR (2002) Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H⁺-ATPase activity in maize roots. Plant Physiology 130:1951-1957.
Canellas LP, Zandonadi DB, Busato JG, Baldotto MA, Simões ML, Martin-Neto L, Façanha AR, Spaccini R, Piccolo A (2008a) Bioactivity and chemical characteristics of humic acids from tropical soils sequence. Soil Science 173:624-637.
Canellas LP, Teixeira Junior LRL, Dobbss LB, Silva CA, Medici LO, Zandonadi DB, Facanha AR (2008b) Humic acids cross interactions with root and organic acids. Annals of Applied Biology 153:157-166.
Carletti P, Masi A, Spolaore B, De Laureto PP, De Zorzi M, Turetta L, Ferretti M, Nardi S (2008) Protein expression changes in maize roots in response to humic substances. Journal of Chemical Ecology 34:804-818.
Chen Y, Aviad T (1990) Effects of humic substances on plant growth. In: MacCarthy P, Clapp CE, Malcom RL, Bloom PR (Eds.), Humic substances in soils and crop science: selected readings. Soil Science Society of America, Madison, pp.161-186.
Chen Y, Clapp CE, Magen H (2004) Mechanisms of plant growth stimulation by humic substances: The role of organo-iron complexes. Soil Science and Plant Nutrition 50:1089-1095.
Clark NA (1926) Plant growth promoting substances, hydrogen ion concentration and the reproduction of Lemna Plant Physiology 1:273.
Darwin C (1880) The power of movement in plants. John Murray, London.
Darwin C (1881) The formation of vegetable mould through the action of worms with some observations on their habits. John Murray, London.
Dell'Agnola G, Nardi S (1987) Hormone-like effect and enhanced nitrate uptake induced by depolycondensed humic fractions obtained from Allolobophoru rosea and A. caliginosa faeces. Biology and Fertility of Soils 4:115-118.
Dobbss LB, Medici LO, Peres LEP, Pino-Nunes LE, Rumjanek VM, Façanha AR, Canellas LP (2007) Changes in root development of Arabidopsis promoted by organic matter from oxisols. Annals of Applied Biology 151:199-211.
Elena A, Diane L, Eva B, Marta F, Roberto B, Zamarreño M, García-Mina JM (2009) 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 Physiology and Biochemistry 47:215-223.
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FAO (2010) Trends in sustainable development. Chemicals, mining, transport and waste management 2010-2011. United Nations, New York.
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Finance ministry, Secretariat for Economic Monitoring (2011) Panorama do mercado de fertilizantes, Maio/2011. Available at: www.seae.fazenda.gov.br
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Instituto de Pesquisa Econômica Aplicada (IPEA) Comunicado nº 145 - Plano Nacional de Resíduos Sólidos: diagnóstico dos resíduos urbanos, agrosilvopastoris e a questão dos catadores. Avaiable at: http://www.ipea.gov.br/portal/images/stories/PDFs/comunicado/120425_comunicadoipea0145.pdf
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Publication Dates

Publication in this collection
23 June 2015
Date of issue
2013

History

Received
26 Feb 2013
Accepted
11 Mar 2013

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] Albuzio A, Ferrari G (1989) Modulation of the molecular size of humic substances by organic acids of the root exudates. Plant Soil 113:237-241.

[2] Arancon NQ, Pant A, Radovich T, Hue NV, Potter JK, Converse CE (2012) Seed germination and seedling growth of tomato and lettuce as affected by vermicompost water extracts (Teas). HortScience 47:1722-1728.

[3] Arteaga M, Garcés N, Novo R, Guridi F, Pino JA, Acosta M, Pasos M, Besú D (2007) Influencia de la aplicación foliar del bioestimulante Liplant sobre algunos indicadores biológicos del suelo. Revista de Protección Vegetal 22:110-117.

[4] Bottomley WB (1914) Some accessory factors in plant growth and nutrition. Proceedings of the Royal Society of London-B 88:237-247.

[5] Bottomley WB (1915) A bacterial test for plant food accessories: (auximones). Proceedings of the Royal Society of London-B 89:102-108

[6] Bottomley WB (1917) Some effects of organic growth-promoting substances: (auximones) on the growth of Lemna minor in mineral culture solutions. Proceedings of the Royal Society of London-B 89:481-507.

[7] Busato JG, Lima L, Aguiar NO, Canellas LP, Olivares FL (2012) Changes in labile phosphorus forms during maturation of vermicompost enriched with phosphorus-solubilizing and diazotrophic bacteria. Bioresource Technology 110:390-395.

[8] Cacco G, Dell'Agnola G (1984) Plant growth regulator activity of soluble humic complex. Canadian Journal of Soil Science 62:306-310.

[9] Cameron RS, Thornton BK, Swift RS, Posner AM (1972) Molecular weight and shape of humic acid from sedimentation and diffusion measurements on fractionated extracts. Journal of Soil Science 23:394-408.

[10] Campos-Cuevas JC, Pelagio-Flores R, Raya-González J, Méndez-Bravo A, Ortiz-Castro R, López-Bucio J (2008) Tissue culture of Arabidopsis thaliana explants reveals a stimulatory effect of alkamides on adventitious root formation and nitric oxide accumulation. Plant Science 174:165-173.

[11] Canellas LP, Olivares FL, Okorokova-Façanha AL, Façanha AR (2002) Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H⁺-ATPase activity in maize roots. Plant Physiology 130:1951-1957.

[12] Canellas LP, Zandonadi DB, Busato JG, Baldotto MA, Simões ML, Martin-Neto L, Façanha AR, Spaccini R, Piccolo A (2008a) Bioactivity and chemical characteristics of humic acids from tropical soils sequence. Soil Science 173:624-637.

[13] Canellas LP, Teixeira Junior LRL, Dobbss LB, Silva CA, Medici LO, Zandonadi DB, Facanha AR (2008b) Humic acids cross interactions with root and organic acids. Annals of Applied Biology 153:157-166.

[14] Carletti P, Masi A, Spolaore B, De Laureto PP, De Zorzi M, Turetta L, Ferretti M, Nardi S (2008) Protein expression changes in maize roots in response to humic substances. Journal of Chemical Ecology 34:804-818.

[15] Chen Y, Aviad T (1990) Effects of humic substances on plant growth. In: MacCarthy P, Clapp CE, Malcom RL, Bloom PR (Eds.), Humic substances in soils and crop science: selected readings. Soil Science Society of America, Madison, pp.161-186.

[16] Chen Y, Clapp CE, Magen H (2004) Mechanisms of plant growth stimulation by humic substances: The role of organo-iron complexes. Soil Science and Plant Nutrition 50:1089-1095.

[17] Clark NA (1926) Plant growth promoting substances, hydrogen ion concentration and the reproduction of Lemna Plant Physiology 1:273.

[18] Darwin C (1880) The power of movement in plants. John Murray, London.

[19] Darwin C (1881) The formation of vegetable mould through the action of worms with some observations on their habits. John Murray, London.

[20] Dell'Agnola G, Nardi S (1987) Hormone-like effect and enhanced nitrate uptake induced by depolycondensed humic fractions obtained from Allolobophoru rosea and A. caliginosa faeces. Biology and Fertility of Soils 4:115-118.

[21] Dobbss LB, Medici LO, Peres LEP, Pino-Nunes LE, Rumjanek VM, Façanha AR, Canellas LP (2007) Changes in root development of Arabidopsis promoted by organic matter from oxisols. Annals of Applied Biology 151:199-211.

[22] Elena A, Diane L, Eva B, Marta F, Roberto B, Zamarreño M, García-Mina JM (2009) 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 Physiology and Biochemistry 47:215-223.

[23] Façanha AR, Façanha ALO, Olivares FL, Guridi F, Santos GA, Velloso ACX, Rumjanek VM, Brasil F, Schripsema J, Braz-Filho R, Oliveira MA, Canellas LP (2002) Bioatividade de ácidos húmicos: efeito sobre o desenvolvimento radicular e sobre a bomba de prótons da membrana plasmática. Pesquisa Agropecuária Brasileira 37:1301-1310.

[24] FAO (2010) Trends in sustainable development. Chemicals, mining, transport and waste management 2010-2011. United Nations, New York.

[25] Fialová S (1969) Influence of sodium humate and nutritive conditions on the content of nucleic acids, particularly on the ribosomal ribonucleic acid in wheat root. Biologia Plantarum 11:8-22.

[26] Finance ministry, Secretariat for Economic Monitoring (2011) Panorama do mercado de fertilizantes, Maio/2011. Available at: www.seae.fazenda.gov.br

[27] Frías I, Caldeira MT, Pérez-Castiñeira JR, Navarro-Aviñó JP, Culiañez-Maciá FA, Kuppinger O, Stransky H, Pagés M, Hager A, Serrano R (1996) A major isoform of the maize plasma membrane H(+)-ATPase: characterization and induction by auxin in coleoptiles. Plant Cell 8:1533-1544.

[28] Gaxiola RA, Sanchez CA, Paez-Valencia J, Ayre BG, Elser JJ (2012). Genetic manipulation of a vacuolar H⁺-PPase: from salt tolerance to yield enhancement under phosphorus-deficient soils. Plant Physiology 159:3-11.

[29] Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Letters 581:2204-2214.

[30] Guminski S (1968) Present-day views on physiological effects induced in plant organisms by humic compounds. Soviet Soil Science 9:1250-1256.

[31] Gutiérrez-Miceli FA, Llaven MAO, Nazar PM, Sesma BR, Álvarez-Solís JD, Dendooven L (2011) Optimization of vermicompost and worm-bed leachate for the organic cultivation of radish. Journal of Plant Nutrition 34:1642-1653.

[32] Hager A, Menzel H, Krauss A (1971) Experiments and hypothesis concerning the primary action of auxin in elongation growth. Planta 100:47-75.

[33] Herder GD, Van Isterdael G, Beeckman T, De Smet I (2010) The roots of a new green revolution. Trends in Plant Science 15:600-607.

[34] Hoben JP, Gehl RJ, Millar N, Grace PR, Robertson GP (2011) Non-linear nitrous oxide (N₂O) response to nitrogen fertilizer in on-farm corn crops of the U.S. Midwest. Global Change Biology 17:1140-1152.

[35] Kogl F, Haagen-Smit A J (1931) Uber die chemie des wuchsstoffs. Proceedings of the Koninklijke Nederlandse Akademie Van Wetenschappen 34:1411-1416.

[36] Instituto de Pesquisa Econômica Aplicada (IPEA) Comunicado nº 145 - Plano Nacional de Resíduos Sólidos: diagnóstico dos resíduos urbanos, agrosilvopastoris e a questão dos catadores. Avaiable at: http://www.ipea.gov.br/portal/images/stories/PDFs/comunicado/120425_comunicadoipea0145.pdf

[37] Li J, Yang H, Peer WA, Richter G, Blakeslee J, Bandyopadhyay A, Titapiwantakun B, Undurraga S, Khodakovskaya M, Richards EL, Krizek B, Murphy AS, Gilroy S, Gaxiola R (2005) Arabidopsis H⁺-PPase AVP1 regulates auxin-mediated organ development. Science. 310:121-125.

[38] Lopes AS, Cox FR (1977) A survey of the fertility status of surface soils under cerrado' vegetation in Brazil. Soil Science Society of America Journal J 41:741-747.

[39] Maggioni A, Varanini Z, Nardi S, Pinton R (1987) Action of soil humic matter on plant roots: Stimulation of ion uptake and effects on (Mg²⁺/K⁺) ATPase activity. Science of the Total Environment 62:355-363.

[40] Malcom RE, Vaughan D (1979) Humic substances and phosphatase activities in plant tissues. Soil Biology and Biochemistry 11:253-259.

[41] Marré E, Ballarin-Denti A (1985) The proton pumps of the plasmalemma and the tonoplast of higher plants. Journal of Bioenergetics and Biomembranes 17:1-21.

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Plant physiology as affected by humified organic matter

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